Botanical Studies (2009) 50: 73-87.

*

Corresponding author: E-mail: hjlin@dragon.nchu.edu.tw;

Tel: +886-4-22840416; Fax: +886-4-22874740.

INTRODUCTION

Agriculture in a particular catchment area is considered

among the most-serious threats to the streams within

that area (Squires and Saoud 1986; Johnson et al., 1997;

Wilby et al., 1998). There are positive relationships

between stream nutrient concentrations and the area

under agriculture (Leland and Porter, 2000; Rhodes et al.,

2001; Kao and Chiu, 2004; Inwood et al., 2005). Nutrient

loading from agricultural land is 10-20 times the load from

forested land (Rekolainen, 1989; Pekarova and Pekar,

1996). Agricultural runoff can lead to higher nutrient

concentrations in nearby streams (Chetelat et al., 1999;

Pan et al., 1999; Dodds et al., 2002) and to an acceleration

of eutrophication (Rekolainen, 1989; Soranno et al., 1996).

Although eutrophic impacts are thought to be greater in

the tropics than at higher latitudes (Downing et al., 1999),

studies of how agriculture effects tropical/subtropical

streams are still very scarce.

Attached algae are often regulated by a variety of

factors, such as nutrients, discharge, current velocity,

light, grazers, and water temperature (Rosemend et al.,

1993; Pan et al., 1999; Soininen and Kononen, 2004). The

nutrient contents of attached algae often show a positive

correlation with the percent of the catchment area altered

by human activities (Ekholm et al., 2000; Rhodes et al.,

2001). Higher water temperatures resulting from the

removal of riparian vegetation will increase attached algae

abundance (Dodds et al., 2002), which may be 2-4-times

higher in clear-cut streams than at other sites (Hill and

Knight, 1988; Kiffney and Bull, 2000). However, little is

known about the response of attached algae to agricultural

land use in tropical/subtropical streams.

In Taiwan, many catchments of mountain streams at

>1,500 m elevation have been developed for farming

fruits and vegetables. The Wuling area is located in the

upstream reaches of the Dajia River of central Taiwan

at about 1,800 m in elevation, comprising three third-

order streams: Cijiawan Stream, Yousheng Stream and

Gaoshan Stream (Figure 1). They are characterized

by having short, straight, steep channels and are often

influenced by fluctuations in precipitation and typhoons.

The catchment of Gaoshan Stream is vegetated by natural

forests. The catchments of the Cijiawan and Yousheng

Streams have each been developed for agriculture, but it

is more intensive in the catchment of Yousheng Stream.

The Cijiawan and Gaoshan Streams are the only habitats

of the endangered Taiwanese masu salmon (Oncorhynchus

masou formosanus).

An early warning system to indicate

Effects of agriculture on the abundance and community

structure of epilithic algae in mountain streams of

subtropical Taiwan

Shu-Fen YU

and Hsing-Juh LIN*

Department of Life Sciences, National Chung Hsing University, Taichung 402, Taiwan

(Received November 1, 2007; Accepted September 16, 2008)

ABSTRACT.

This study aimed to characterize the abundance and community structure of epilithic algae and

to examine the effects of intensive agriculture in mountain streams of the Wuling area. There were significant

seasonal variations in epilithic algal biomass, with higher values in spring and winter and lower values in

summer and fall. Effects of agriculture on the subtropical streams of the Wuling area were significant and

varied with the extent of agriculture in the catchment. The biomass was significantly higher in Yousheng

Stream with a larger area of agriculture than in other streams. Diatoms were the most abundant species,

contributing over 85% to the total cell number. Most of these were pennatae diatoms, of which the genus

Achnanthidium was the most abundant in the area. However, the communities showed clear seasonal and

spatial changes. BIOENV analysis suggested that the combination of water temperature, conductivity ,

NO

2

+NO

3

and SiO

2

concentrations and current velocity

comprised the major factors explaining seasonal

changes in the community, while the combination of NO

2

+NO

3

and SiO

2

concentration and grazer density

comprised the major factors affecting spatial changes. Changes in abundance and community structure of

epilithic algae can be used to monitor the effects of agriculture in tropical/subtropical mountain streams.

Keywords: Achnanthidium; Current velocity; Diatoms; Grazer density; NO

2

+NO

3

; Wuling.

ECOlOgy

74

Botanical Studies, Vol. 50, 2009

if the streams in the Wuling area are changing due to

agriculture is required. Comparative studies of the three

streams with their different degrees of local agriculture

would be helpful in determining the effects of agriculture

on tropical/subtropical streams. The aims of the present

study were: (1) to characterize the biomass and community

structure of epilithic algae in the streams of the Wuling

area; (2) to examine the effects of agriculture on this

biomass and community structure.

MATERIAlS AND METHODS

Study sites

In total, twelve sites were sampled in the streams of the

Wuling area (Figure 1). The stream beds contain abundant

rocks, primarily deposited by the weathering of sandstone

and slate. The mean water temperature was 12¢XC, ranging

from 18¢XC in summer to 10¢XC in winter. Climatic data

derived from a local weather station (Wuling) during

2003-2004 (Climatological Data Annual Report, Central

Weather Bureau of Taiwan) showed that in the dry season

of October-April, the mean monthly rainfall normally

does not exceed 40 mm, and that in the wet season of

May-September, the average monthly rainfall frequently

exceeds 150 mm. The mean discharge in the dry season

was 1.84-2.30 m

3

s

-1

and in the wet season was 2.58-2.96

m

3

s

-1

(Chung et al., 2008).

Gaoshan Stream is 10.6 km long with a mean gradient

of 140 m/km and a catchment area of 40 km

2

. The stream

bed is dominated by pebble (39%) and rubble (27%) in

winter, but consists of a high proportion of boulders (44%)

in summer (Yeh, 2006).

This catchment is vegetated

by natural forests, and no agriculture is present (Wang,

1989), so the stream is assumed to be in a pristine state.

Cijiawan Stream is 15.3 km long with a mean gradient of

130 m/km and a catchment area of 76 km

2

. The stream bed

consists of a high proportion of pebble (42%) in winter,

but is dominated by rubble (26%) and boulders (21%)

in summer (Yeh, 2006). The upper reach of Cijiawan

Stream is bordered by riparian forest, but the lower reach

has been developed for agriculture, including an area of

104 ha of vegetables, apples, peaches, and pears. It is

considered to be moderately influenced by agriculture.

Yousheng Stream is 11.4 km long with a mean gradient of

68 m/km and a catchment area of 31 km

2

. The substrate

is dominated by gravel (39%) and pebble (39%) (Yeh,

2006).

The entire reach with an area of 295 ha has been

intensively developed for farming vegetables since the

1970s. The stream has been channelized, and the natural

riparian vegetation has been almost completely removed.

It is regarded as highly influenced by agriculture. Canopy

cover was higher in the Gaoshan Stream (90%) and the

upper reach of the Cijiawan Stream (86%), and it was

lower in the lower reach of the Cijiawan (57%) and

Yousheng Streams (50%).

Sample collection

Riffles are the major habitat in the streams of the

Wuling area. Attached algae samples were collected

monthly from randomly selected rocks (n = 5) in the riffle

zone of streams at 7:00-10:00 am from March 2003 to

March 2004. On each rock, a frame made of steel was

used to define a sampling area of an algal patch of 12.5

cm

2

,

and four algal patches were scraped off a surface area

of 50 cm

2

with a toothbrush. The scraped algae were then

washed off the toothbrush and rocks with 50-100 mL of

filtered stream water. In the laboratory, the algal samples

were centrifuged for 10 min to concentrate them to 5 mL.

A 3-mL subsample was extracted for chlorophyll a in 90%

acetone (Lobban et al., 1988). The other 2-mL subsample

was fixed in Lugol¡¦s solution for taxon identification.

The taxon was identified and counted using a light

microscope of Differential Interference Contrast (Zeiss

Axioplan 2). Filamentous algae such as Oscillatoria

and Cladophora were counted in every cell with a

hemocytometer. Diatom samples were further treated with

H

2

SO

4

and KNO

3

(Sabater et al., 1990) and mounted with

Naphrax. At least 500 diatom valves were counted per

sample. Identification was carried out according to Patrick

and Reimer (1966), Patrick and Reimer (1975), Round et

al. (1990), Vyverman (1991), Yamagishi (1992), Round

and Bukhtiyarova (1996), and Krammer and Lange-

Bertalot (1997).

On each sampling occasion, water temperature, pH,

conductivity, turbidity, dissolved oxygen (DO), and

current velocity of the stream were measured in situ with

Figure 1. Sampling sites and agricultural areas (black circles) in

the streams of the Wuling area.

YU and LIN ¡X Effects of agriculture on epilithic algae

75

portable meters (YSI 6560 multiparameter monitoring

sensors and Son Tek Flow Tracker Handheld ADV) at

7:00-10:00 am. Water samples for other chemical factors

were immediately placed on ice in a cooler and brought

back to the laboratory for analyses of nitrite (NO

2

-

) and

nitrate (NO

3

-

), total phosphorus (TP), biological oxygen

demand (BOD), and SiO

2

following the standard methods

of APHA (Clesceri et al., 1998). Density of grazers

including Ephemeroptera and Trichoptera was determined

by collecting with Suber net sampler (30.5 ¡Ñ 30.5 cm) by

Kuo and Chiu (2004; 2005).

Data analysis

Shannon-Weiner diversity indices (H¡¦) were calculated

using natural logs as indices of epilithic algal communities.

A two-way fixed ANOVA model was used to determine

whether environmental factors, epilithic algal biomass

in terms of chlorophyll a or Shannon-Weiner diversity

indices significantly differed among study sites or among

seasons. Before the analyses, values of chlorophyll a were

log-transformed (Clarke and Warwick, 1994) to conform

to normality and homogeneity of variance assumptions. If

the results of the ANOVA indicated significant treatment

effects at the 0.05 probability level (p), then Fisher¡¦s

protected least significant difference (LSD) test was used

to determine which means significantly differed. The

relationships of abundance of the epilithic algal taxon with

environmental variables were determined using Spearman

rank correlations.

In order to reveal spatial and seasonal patterns of the

epilithic algal community, species compositions were

studied using multivariate analyses in the PRIMER

(vers. 5.2) computer package (Clarke and Gorley,

2001). The Bray-Curtis coefficient was used to produce

a similarity matrix of species composition between

any two samples according to the cell number of each

taxon. Cell numbers were log-transformed to reduce the

weighting of the dominant taxon in the communities

(Krebs, 1999). The similarity matrix was first classified

by hierarchical agglomerative clustering using the

unweighted pair group mean arithmetic (UPGMA) linking

method, and it was then ordinated using non-metric

multidimensional scaling (MDS) techniques. A two-way

crossed ANOSIM (analysis of similarities) was used to

determine whether the effects of site and season on the

community structure were significant by comparing the

observed statistic to its permutation distribution in the

absence of differences (Clarke and Warwick, 1994). If

the results indicated significance at the 0.05 probability

level, pairwise comparisons and the Bonferroni correction

for the significance level were used to determine which

levels differed. Similarity of percentages (SIMPER) was

employed to reveal the most-common taxon in replicate

samples for each group. BIOENV was employed to reveal

the most influential environmental variables affecting

the structure of the epilithic algal community. BIOENV

selects the most influential environmental variable subset

by maximizing the weighted Spearman rank correlation

(£l

w

) between the similarity matrix of species composition

and similarity matrices of a combination of environmental

variables considered at steadily increasing levels of

complexity.

RESUlTS

Environmental variables

For each site, monthly samples were pooled into one

sample. Classification and MDS ordination separated

the epilithic algal communities into four regions (Figure

1), including region I of the upper reach of the Cijiawan

Stream (site A), region II of the lower reach of the

Cijiawan Stream (sites B-F), region III of the Gaoshan

Stream (sites G-I), and region IV of the Yousheng Stream

(sites J-L).

In the Wuling area, water temperature ranged

between 5.1-18.5¢XC (Table 1). DO remained high (>

6.8 mg L

-1

), but turbidity (< 0.68 NTU) and BOD (<

2 mg L

-1

) remained low in all regions. pH values and

conductivity, respectively, averaged 8.3~8.5 and 152-239

£gS cm

-1

. Current velocity was high with an average of

33 -65 cm s

-1

. Concentrations of SiO

2

and TP in the

water column were low and remained 4.18-6.14 and

0.02-0.03 mg L

-1

,

respectively, in all regions. However,

NO

2

+NO

3

concentrations corresponded well with the area

of agriculture in the catchment of the streams. NO

2

+NO

3

concentrations were high in the lower reaches of the

Cijiawan Stream and even higher in the Yousheng Stream.

The mean NO

2

+NO

3

concentration reached 5.65 mg L

-1

in

the Yousheng Stream. Mean canopy cover was 50%-90%.

Grazer density averaged 261-839 individual m

-2

.

Water temperature, turbidity, conductivity, current

velocity, and grazer density underwent significant seasonal

and regional changes (Table 2). Water temperature was

higher in summer (18.5¢XC) and lower in winter (5.1¢XC). It

was higher in the Yousheng Stream which lacked a canopy

due to the agricultural activity, and lower in the Gaoshan

Stream which had a high canopy. Turbidity was higher

in the Yousheng Stream and lower in the upper reach of

the Cijiawan Stream. It was higher in spring and lower in

fall. Yousheng Stream and the upper reach of the Cijiawan

Stream possessed greater conductivity values than other

regions. The greatest conductivity value was observed in

winter when the discharge was small. Current velocity

was fastest in Gaoshan Stream, followed by the lower

reach of Cijiawan Stream and Yousheng Stream, and was

slowest in the upper reach of Cijiawan Stream. It was

faster in summer and fall and slower in winter and spring.

Grazer density was greater in Cijiawan Stream and lower

in Gaoshan Stream and Yousheng Stream. It was greater in

fall and winter and lower in spring and summer.

Nutrient concentrations also showed significant

seasonal and regional changes (Table 2)

.

TP concentrations

did not differ among the regions. Concentrations of

NO

2

+NO

3

were higher in Yousheng Stream, and the

76

Botanical Studies, Vol. 50, 2009

mean value was 6-8-times that of other regions. SiO

2

concentrations were higher in the upper reach of

Cijiawan and Gaoshan Streams. In general, these nutrient

concentrations were higher in summer and fall and lower

in winter and spring.

Epilithic algal community and biomass

Diatoms were the most dominant taxa of the epilithic

algal communities in the streams of the Wuling area. Of

114 taxa identified, 107 taxa were diatoms, followed by

cyanobacteria and Chlorophyta. Diatoms contributed

85% of the total cell numbers of the algal communities.

Most diatoms belonged to pennatae genera, and > 40%

of the genera were of Achnanthidium. A. atomus, A.

minutissimus, and Platessa hustedtii were the most

abundant species.

Samples from all study sites were also pooled into

monthly samples of combined sites. Classification and

MDS ordination of the cell number of each taxon of

the communities separated the monthly samples into

four seasonal categories (Figure 2). The winter category

contained samples collected during the period of

December 2003 to February 2004; the spring category

comprised samples from March 2004 and March 2003;

the summer category was from April 2003 to October

2003; and the fall category was from November 2003.

Table 1. Environmental variables and grazer density of the four regions collected from March 2003 to March 2004 in the Wuling

area. Values are presented as the mean¡ÓSD with the range in parentheses.

Site group

I

II

III

IV

Water temperature (¢XC)

11.8¡Ó2.4

11.8¡Ó2.4

11.2¡Ó2.8

12.8¡Ó3.3

(7.4-15.5)

(5.1-16.5)

(5.1-15.2)

(8.0-18.5)

DO (mg/L)

9.8¡Ó1.2

9.9¡Ó1.4

10.3¡Ó1.2

10.1¡Ó1.2

(7.5-11.4)

(6.9-13.2)

(7.0-13.0)

(6.8-12.2)

Turbidity (NTU)

0.14¡Ó0.11

0.19¡Ó0.17

0.24¡Ó0.18

0.34¡Ó0.23

(0.01-0.35)

(0.01-0.67)

(0.01-0.62)

(0.02-0.68)

BOD (mg/L)

0.60¡Ó0.39

0.61¡Ó0.33

0.62¡Ó0.40

0.69¡Ó0.42

(0.03-1.40)

(0.00-1.32)

(0.05-1.70)

(0.01-1.59)

pH

8.5¡Ó0.3

8.3 ¡Ó0.3

8.3 ¡Ó0.2

8.3¡Ó0.6

(8.1-9.1)

(7.7-9.2 )

(7.9 -8.9)

(7.1-9.1)

Conductivity (£gS/cm)

233¡Ó45

152¡Ó36

152¡Ó27

239¡Ó72

(200-350)

(90-230)

(125-210)

(130-390)

Current velocity (cm/s)

33¡Ó15

55 ¡Ó29

65¡Ó26

53 ¡Ó27

(15-60 )

(14 -123)

(55-122 )

(16-94 )

SiO

2

(mg/L)

6.14¡Ó0.74

4.18¡Ó0.81

4.99¡Ó0.72

4.53¡Ó0.87

(5.00-7.01)

(2.70 - 6.43)

(3.66-6.61)

(2.80-6.04)

NO

2

+NO

3

(mg/L)

0.24¡Ó0.14

0.70¡Ó0.60

0.26¡Ó0.39

5.65¡Ó3.84

(0.11-0.62)

(0.10-2.91)

(0.04-2.22)

(0.26-18.66)

Total P (mg/L)

0.02¡Ó0.02

0.02¡Ó0.03

0.03¡Ó0.05

0.02¡Ó0.02

(0.00-0.06)

(0.00-0.17)

(0.00-0.19)

(0.00-0.11)

Grazer density (individual/m

2

)

839¡Ó354

743¡Ó417

310¡Ó179

261¡Ó203

(191-1444)

(69-1794)

(152-739)

(54-680)

Region I: the upper reach of Cijiawan Stream, region II: the lower reach of Cijiawan Stream, region III: Gaoshan Stream and region

IV: Yousheng Stream.

YU and LIN ¡X Effects of agriculture on epilithic algae

77

Table 2. Two-way ANOVA (site ¡Ñ season) of environmental variables and grazer density collected from the four regions in different

seasons in the Wuling area. If the results of the ANOVA indicated significant treatment effects at the 0.05 probability level (p),

then Fisher¡¦s protected LSD test was used to determine which means significantly differed. Means with the same letter do not

significantly differ.

Source

df

F value

Pr > F

Water temperature

Site

3

5.01

0.003 IV

a

I

ab

II

ab

III

b

Season

3

69.95

< 0.001 Summer

a

Fall

b

Spring

c

Winter

d

Site ¡Ñ Season

9

0.85

0.575

DO

Site

3

1.01

0.389

Season

3

0.35

0.790

Site ¡Ñ Season

9

1.90

0.057

Turbidity

Site

3

7.88

< 0.001 IV

a

III

b

II

bc

I

c

Season

3

13.22

< 0.001 Spring

a

Winter

b

Summer

b

Fall

c

Site ¡Ñ Season

9

0.22

0.992

BOD

Site

3

0.38

0.764

Season

3

0.77

0.514

Site ¡Ñ Season

9

0.66

0.742

pH

Site

3

0.69

0.560

Season

3

2.63

0.053

Site ¡Ñ Season

9

0.37

0.946

Conductivity

Site

3

43.86

< 0.001 IV

a

I

a

II

b

III

b

Season

3

7.70

< 0.001 Winter

a

Spring

b

Summer

b

Fall

b

Site ¡Ñ Season

9

1.13

0.348

Current velocity

Site

3

17.06

< 0.001 III

a

II

b

IV

c

I

c

Season

3

9.22

< 0.001 Summer

a

Fall

ab

Winter

bc

Spring

c

Site ¡Ñ Season

9

1.27

0.260

SiO

2

Site

3

45.00

< 0.001 I

a

III

b

IV

c

II

d

Season

3

42.66

< 0.001 Fall

a

Summer

a

Spring

b

Winter

c

Site ¡Ñ Season

9

0.85

0.568

NO

2

+NO

3

Site

3

59.88

< 0.001 IV

a

II

b

III

b

I

b

Season

3

4.48

0.005 Summer

a

Winter

ab

Spring

b

Fall

b

Site ¡Ñ Season

9

8.35

< 0.001

TP

Site

3

0.79

0.501

Season

3

5.98

0.001 Fall

a

Summer

a

Winter

b

Spring

b

Site ¡Ñ Season

9

0.28

0.979

Grazer density

Site

3

22.33

< 0.001 I

a

II

b

III

c

IV

c

Season

3

3.18

0.026 Fall

a

Winter

ab

Summer

b

Spring

b

Site ¡Ñ Season

9

0.73

0.682

df = degree of freedom. Region I: the upper reach of Cijiawan Stream, region II: the lower reach of Cijiawan Stream, region III:

Gaoshan Stream and region IV: Yousheng Stream.

78

Botanical Studies, Vol. 50, 2009

The MDS ordination (stress = 0.07) revealed a clear and

gradual seasonal shift in species composition from April

2003 to April 2004 in a counter-clockwise direction.

There appeared to be a rapid shift in the epilithic algae

communities from November (fall) to December (winter).

ANOSIM analysis demonstrated significant differences

in epilithic algae communities among seasons (R = 0.36,

p = 0.001). The pairwise comparisons further showed that

the epilithic algae communities sampled in winter could

be separated from those sampled in summer (R = 0.55, p =

0.001), fall (R = 0.36, p = 0.001), and spring (R = 0.28, p =

0.001).

The species richness of the epilithic algal communities

was higher in Yousheng Stream, with its intense exposure

to agricultural influences, than in other regions.

Shannon-

Wiener diversity indices of the epilithic algal communities

revealed significant seasonal and regional differences. The

Shannon-Weiner diversity indices were significantly higher

in Yousheng Stream (1.85 ¡Ó 0.50) than in Gaoshan Stream

(1.79 ¡Ó 0.36). The lower reach of Cijiawan Stream had the

lowest diversity indices (1.62 ¡Ó 0.47). Diversity indices

were significantly higher in fall (1.85 ¡Ó 0.41) and summer

(1.79 ¡Ó 0.47) than in winter (1.70 ¡Ó 0.42) or spring (1.62 ¡Ó

0.47).

SIMPER analysis showed that mean similarity

between any two regions was relatively lower in region

IV (Yousheng Stream) with region I, II and III (Table 3).

Region I (upper reach of Cijiawan Steam) and region II

(lower reach of Cijiawan Steam) had a higher similarity.

The mean similarity between winter and other seasons

was lower than that between other seasons and each

other (Table 4). There was a relatively higher similarity

between summer and fall. The mean similarity of the algal

communities within each season was relatively lower in

spring and higher in fall, indicating that the variability

among replicated samples was greater in spring (Table

5). The seasonal shift in the epilithic algal communities

in the Wuling area could be illustrated by changes in the

relative abundances of the six most distinct taxa in each

season, including the diatoms A. atomus, A. minutissimum,

P. hustedtii, Cocconeis placentula and Planothidium

lanceolatum, and the cyanobacteria Oscillatoria spp.

A. atomus was the most frequently observed taxon year

round, but it occurred more frequently in spring and less

in fall. P. hustedtii also occurred year round, but was more

frequently observed in fall and winter. A. minutissimum

and P. lanceolatum

also occurred year round, but showed

unclear seasonal changes. C. placentula occurred more

frequently in summer and fall, but disappeared in

winter. The cyanobacteria including Oscillatoria spp.,

Chroococcus spp. and Lyngbya sp. and the chlorophyte

Cladophora sp. also occurred more frequently in winter.

Achnanthidium, Cocconeis, and Planothidium were

the most frequently observed genera of the epilithic

algal communities in all of the regions examined in the

Wuling area (Table 6). In the region I (upper reach of

Cijiawan Steam), the two diatom genera Cocconeis and

Navicula occurred more frequently than in other regions.

The cyanobacteria Chroococcus spp., Lyngbya sp. and

Oscillatoria spp. occurred more frequently in the region

II (lower reach of Cijiawan Steam) than in other regions.

In the region III (Gaoshan Stream), no cyanobacteria were

observed, but Gomphonema was the most representative

diatom genus. The diatoms Cymbella cymbiformis

var. nonpunctata, Cymbella sp1., Diatoma vulgaris,

Encyonema minutum, Nitzschia sinuata var. tabellaria,

and Nitzschia sp1. occurred more frequently in Yousheng

Stream than in other regions.

Epilithic algal biomass in terms of chlorophyll a also

showed significant seasonal and regional differences

(Figure 3). However, season and region showed a

significant interaction. Chlorophyll a concentrations of

epilithic algae collected from Yousheng Stream increased

more rapidly and became greater in winter and spring,

but no significant difference was detected from other

regions in summer. Mean chlorophyll a concentrations

of epilithic algae in Yousheng Stream reached 320 mg

Figure 2. MDS ordination of Bray-Curtis similarities between

epilithic algal communities collected monthly from March 2003

to March 2004 in the streams of the Wuling area.

Table 3. Mean similarity (%) of epilithic algal communities

between any two regions of the streams in the Wuling area.

I

II

III

IV

I

100

35.7 34.0 29.7

II

100

33.6 29.1

III

100

32.4

IV

100

Table 4. Mean similarity (%) of epilithic algal communities

between any two seasons of the streams in the Wuling area.

Spring Summer Fall Winter

Spring

100 32.9 33.8 29.5

Summer

100 40.1 26.8

Fall

100 29.6

Winter

100

YU and LIN ¡X Effects of agriculture on epilithic algae

79

Table 5. Contribution (%) of species occurrence in seasonal epilithic algal communities in the streams of the Wuling area.

Season

Spring Summer

Fall

Winter

Average similarity within each season

34.8

39.7

46.3

36.4

Species

Bacillariophyta

Achnanthidium atomus (Hust.) O. Monnier, Lange-Bert. Et Ector 22.1

15.5

14.2

16.9

Achnanthidium minutissimum (Kutz.) Czarn.

8.00

6.54

7.85

7.22

Achnanthidium sp.1

3.17

6.15

4.78

3.16

Achnanthidium sp.2

1.68

2.00

Achnanthidium sp.3

1.27

5.81

1.57

Caloneis sp.

10.7

Cocconeis pediculus Ehrenb. var. pediculus

5.17

1.62

2.55

1.45

Cocconeis placentula var. euglypta (Ehrenb.) Grunow

6.10

15.6

13.8

Cymbella affinis Kutz.

4.25

Cymbella sp.1

1.68

1.80

Diatoma hyemalis var. mesodon (Ehrenb.) Grunow

2.03

1.38

Gomphonema dichotomum Kutz. var. dichotomum

1.11

Gomphonema minutum (C. Agardh) C. Agardh

1.23

3.59

Gomphonema occultum E. Reichardt & Lange-Bert.

1.24

1.66

Gomphonema olivaceum (Hornem.) Breb. var. olivaceum

1.70

Gomphonema tergestinum Fricke var. tergestinum

2.68

Gomphonema sp.2

1.63

Navicula cryptocephala Kutz.

1.08

Navicula sp.1

2.58

Navicula sp.2

1.97

1.37

Navicula sp.4

2.11

Nitzschia sinuata var. tabellaria (Grunow) Grunow

1.16

Nitzschia sp.1

1.23

Planothidium lanceolatum (Breb. ex Kutz.) Round & Burkhtiy.

6.98

7.21

8.79

7.16

Platessa hustedtii (Krasske) Lange-Bert.

10.8

9.58

13.8

14.8

Reimeria sinuata (W. Greg.) J.P. Kociolek & Stoermer

1.49

3.6

3.46

Rossithidium pusillum (Grunow) Round & Bukht.

3.74

1.40

Synedra ungeriana var. pseudogaillonii (H. Kobayasi et ldei)

1.25

3.86

Chlorophyta

Cladophora sp.

0.90

Cyanobacteria

Chroococcus spp.

1.74

1.75

0.91

Lyngbya spp.

1.38

2.18

3.84

Oscillatoria spp.

7.11

5.27

3.93

8.41

Total

89.3

90.0

90.3

88.1

80

Botanical Studies, Vol. 50, 2009

m

-2

. The chlorophyll a concentrations collected from

the lower reach of Cijiawan Steam averaged 96 mg m

-2

.

The chlorophyll a concentrations in the upper reach of

Cijiawan Steam and Gaoshan Stream were lower and

averaged 52 mg m

-2

and 82 mg m

-2

,

respectively.

Correlation of epilithic algae with environmental

variables

BIOENV analysis showed that the combination of

water temperature, conductivity, NO

2

+NO

3

and SiO

2

concentrations, and current velocity were the main factors

(£l

w

= 0.688) explaining the seasonal shifts in the epilithic

algal communities in the Wuling area. It also showed that

the combination of NO

2

+NO

3

and SiO

2

concentrations

and grazer density

were the main factors (£l

w

= 0.589)

responsible for the regional variations.

The diatoms A. atomus, Achnanthes sp. 1, Caloneis sp.,

Cymbella, Planothidium, P. hustedtii and Rossithidium

pusillum, the chlorophyte Cladophora sp. and the

cyanobacteria Oscillatoria spp. were negatively correlated

with water temperature (Table 7). Conversely, the

diatoms Cocconeis, Diatoma, Encyonema, Gomphonema,

Navicula, an d Reimeria were positively correlated with

water temperature. Almost all the species were negatively

correlated with current velocity.

A. atomus, Achnanthes sp.

1, G. dichotomum, Achnanthidium, Diatoma, Encyonema,

Gomphonema, Planothidium, and Rossithidium were

negatively correlated with grazer density, while the

cyanobacteria Chroococcus and Oscillatoria were

positively correlated with grazer density. A. atomus, A.

minutissimum, Achnanthes sp. 1., D. vulgaris, E. minutum,

N. sinuata var. tabellaria, Nitzschia sp. 2, Reimeria

sinuate, Synedra ungeriana var. pseudogaillonii, and the

cyanobacteria Nostoc spp. were positively correlated with

NO

2

+NO

3

concentrations. However, C. placentula var.

euglypta, C. cymbiformis var. nonpunctata, Gomphonema

tergestinum var. tergestinum, an d Gomphonema sp.

1 were positively correlated with TP concentrations.

Almost all diatoms were positively correlated with SiO

2

concentrations, but Oscillatoria spp. was negatively

correlated with SiO

2

concentrations.

DISCUSSION

Classification of trophic state in stream systems is most

appropriately based on algal biomass and secondarily

on nutrients (Dodds et al., 1998). Dodds et al. (1998)

suggested the boundary of mean benthic chlorophyll a

concentration for eutrophic stream systems is > 70 mg m

-2

and the boundary between mesotrophic and oligotrophic

systems is 20 mg m

-2

. Mean chlorophyll a concentrations

of epilithic algae in Yousheng Stream (320 mg m

-2

) and

the lower reach of Cijiawan Stream (96 mg m

-2

) were far

beyond the boundary for eutrophic systems. However,

the mean chlorophyll a concentration in Gaoshan Stream

(82 mg m

-2

) was slightly greater than the boundary for

eutrophic systems. The mean chlorophyll a concentration

in the upper reach of Cijiawan Steam (52 mg m

-2

) was

lower than the boundary for eutrophic systems. In

addition, Dodds et al. (1998) suggested the boundary

of mean total nitrogen (TN) concentration for eutrophic

stream systems is > 1500 £gg L

-1

and the boundary between

mesotrophic and oligotrophic systems is < 700 £gg L

-1

.

In

this study, although organic N was not measured due to

low nutrient loading through sewer drains, mean NO

2

+NO

3

concentration in Yousheng Stream (5650 £gg L

-1

) was still

far beyond the boundary for eutrophic stream systems.

Accordingly, the severely agriculturally-influenced

Yousheng Stream (region IV) could be classified as

a eutrophic system. In the lower reach of Cijiawan

Steam (region II), which was moderately influenced by

agriculture, mean NO

2

+NO

3

concentration (700 £gg L

-1

)

was just beyond the boundary for mesotrophic systems.

Mean NO

2

+NO

3

concentrations in the upper reach of

Cijiawan Steam (region I, 240 £gg L

-1

) and Gaoshan Stream

(region III, 260 £gg L

-1

) were far below the boundary

between oligotrophic and mesotrophic systems. These

streams could therefore be classified as oligotrophic or as

reference systems.

The influence of agricultural land use on NO

2

+NO

3

concentrations and epilithic algal biomass is clearly

demonstrated by a comparison of forested and agricultural

regions. The impact of agriculture on the mountain

streams of the Wuling area were significant and varied

with the area of agriculture in the catchment. In the

highly agriculturally-influenced Yousheng Stream,

NO

2

+NO

3

concentrations were extremely high, but not

the concentrations of TP. Epilithic algal biomass was

significantly higher in Yousheng Stream, where NO

2

+NO

3

concentrations were the highest of any stream. NO

2

+NO

3

concentrations were low in the upper reach of Cijiawan

Stream, but increased remarkably in the lower reach after

the stream had passed through the agricultural area (Figure

1). In Japanese agricultural land, the N load of chemical

Figure 3. Monthly changes in epilithic algal chlorophyll a

concentrations (mean¡ÓSD) from March 2003 to March 2004

collected in four regions of the streams in the Wuling area.

Region I: the upper reach of Cijiawan Stream, region II: the

lower reach of Cijiawan Stream, region III: Gaoshan Stream and

region IV: Yousheng Stream.

YU and LIN ¡X Effects of agriculture on epilithic algae

81

Table 6. Contribution (%) of species occurrence in regional epilithic algal community in the streams of the Wuling area.

Region

I

II

III

IV

Average similarity within each region

39.9

38.4

41.6

34.6

Species

Bacillariophyta

Achnanthidium atomus (Hust.) O. Monnier, Lange-Bert. Et Ector

16.1

18.2

17.6

15.5

Achnanthidium minutissimum (Kutz.) Czarn.

6.88

5.04

7.57

12.5

Achnanthidium sp.1

7.13

4.52

7.11

3.11

Achnanthidium sp.2

3.87

1.66

Achnanthidium sp.3

3.51

2.04

0.87

Achnanthes sp.1

2.38

Caloneis sp.

0.91

0.67

Cocconeis pediculus Ehrenb. var. pediculus

5.23

1.48

1.33

3.25

Cocconeis placentula var. euglypta (Ehrenb.) Grunow

15.12 9.22

7.53

6.07

Cymbella sp.1

1.10

Cymbella cymbiformis var. nonpunctata Font.

0.91

Diatoma hyemalis var. mesodon (Ehrenb.) Grunow

2.64

1.01

0.60

Diatoma vulgaris Bory var. vulgare

3.99

Encyonema minutum (Hilse ex Rab.) D.G. Mann

1.99

Gomphonema dichotomum Kutz var. dichotomum

1.80

Gomphonema minutum (C. Agardh) C. Agardh

0.83

4.76

1.56

Gomphonema occultum E. Reichardt & Lange-Bert.

1.63

Gomphonema parvulum (Kutz.) Kutz.

1.25

0.61

Gomphonema tergestinum Fricke var. tergestinum

3.40

1.73

Gomphonema sp.1

1.38

Navicula angusta Grunow

1.44

0.98

Navicula menisculus Schum.

1.07

Navicula sp.1

1.04

Navicula sp.2

2.29

1.30

1.33

0.72

Navicula sp.3

0.97

Nitzschia sinuata var. tabellaria (Grunow) Grunow

0.89

Nitzschia sp.2

1.75

Planothidium lanceolatum (Breb. ex Kutz.) Round & Burkhtiy.

9.76

5.55

11.4

6.65

Platessa hustedtii (Krasske) Lange-Bert.

7.61

11.9

15.3

8.88

Reimeria sinuata (W. Greg.) J.P. Kociolek & Stoermer

2.48

1.25

2.08

Rossithidium pusillum (Grunow) Round & Bukht.

2.05

0.92

Synedra ungeriana var. pseudogaillonii (H. Kobayasi et ldei)

0.90

0.93

2.54

Cyanobacteria

Chroococcus spp.

4.71

Lyngbya spp.

5.70

Nostoc spp.

0.93

Oscillatoria spp.

8.62

14.9

2.22

Total

90.3

90.7

90.5

87.1

82

Botanical Studies, Vol. 50, 2009

YU and LIN ¡X Effects of agriculture on epilithic algae

83

agricultural fertilizers reached 59% of the total N load

(Kunikane and Magara, 1984). The increases in NO

2

+NO

3

concentrations are indicative of runoff from agriculture in

the catchment. The NO

2

+NO

3

concentration in Yousheng

Stream is significantly higher than that of the Cijiawan and

Gaoshan Streams, reflecting the high levels of fertilizers

applied to agricultural land in comparison with other

regions.

N, but not P, was found to stimulate attached algal

production in subtropical streams with sufficient light

(Mosisch et al., 2001). Filamentous green algae was also

observed more frequently in open streams subject to

high irradiance. Yousheng Stream basin had been clear

cut, and the NO

2

+NO

3

concentrations and chlorophyll

a values significantly exceeded other regions. It thus

had more filamentous green algae than other regions.

Moreover, turbidity was also higher in Yousheng Stream

and the lower reach of Cijiawan Stream. However, in

Gaoshan Stream, bordered by riparian forests, NO

2

+NO

3

concentrations and water temperatures remained low.

Hill and Knight (1988) indicated that removal of riparian

vegetation may change the amount of sunlight reaching

the stream surface and thus the water temperature. In

the upper Michigan River, forests were associated with

lower stream NO

3

concentrations (Inwood et al., 2005).

Our results suggest that clearing forests for agriculture in

the catchment of subtropical streams not only increases

NO

2

+NO

3

concentrations, but also substantially increases

erosion and sediment load from slope lands (Hornung and

Newson, 1986) and water temperature.

Dissolved silicate

in streams usually comes from

mineral soils and bedrock, and the concentrations are

higher in headwaters of the catchment. Detenbeck et

al. (2003) indicated that SiO

2

concentrations in streams

would decrease by reducing contact with mineral soils and

bedrock in a stream system with high catchment storage,

which is defined as the fraction of the catchment area

covered by lakes and wetlands. In this study, we found

that SiO

2

concentrations were lower in the agriculture-

influenced Yousheng Stream and the lower reach of

Cijiawan Stream. It appears that agriculture in the

catchment reduced the inflow of dissolved silicate from

mineral soils and bedrock into the streams. Dissolved

silicate is known to be a main limiting factor for diatoms.

In this study, we also found that almost all diatoms were

positively correlated with SiO

2

. Therefore, diatoms were

relatively less abundant in the agriculturally-influenced

regions and in winter and fall when the discharge and SiO

2

concentrations were lower in the Wuling area.

The tropical/subtropical monsoon climate in Taiwan

is characterized by abundant rainfall in summer and

dryness in winter. Streams of the Wuling area are thus

dominated by flow regimes. Running waters in monsoon

Asia often show distinct seasonality (Cusing et al., 1995).

A lower stream discharge was found to result in greater

attached algae biomass (Kishi et al., 2004). In mountain

streams of the Wuling area, the discharge in the dry

84

Botanical Studies, Vol. 50, 2009

season of October-April was < 5 m

3

s

-1

, and the current

velocity was relatively slow (15 cm s

-1

). In the wet season

of May-September, the discharge increased to > 10 m

3

s

-1

, and the current velocity reached > 60 cm s

-1

. These

facts might explain why cyanobacteria and chlorophytes

were observed more frequently in winter when the

current velocity was slower. Moreover, typhoons and

thunderstorms often bring floods in summer. Consequently,

the discharge became 20 m

3

s

-1

, and the current velocity

reached 122 cm s

-1

, which might have reset the attached

algae communities to earlier successional stages (Oemke

and Burton, 1986). The fast current velocity and changing

flow regime have likely resulted in the dominance of

small-sized diatoms such as Achnanthes, Achnanthidium,

and Cocconeis in the streams especially in summer and

fall. These small-sized diatoms are generally characterized

by prostrate or crustose forms which tightly adhere to the

substrate to resist detachment by flooding (Leland and

Porter, 2000).

Despite this, classification and MDS ordination of the

epilithic algal communities in streams of the Wuling area

clearly reflected the effects of agriculture in the catchment.

The epilithic algal communities were primarily affected

by NO

2

+NO

3

concentrations in the streams resulting

from agricultural runoff, and our conclusion is similar

to the findings of Rosemond et al. (1993) and Dodds

et al. (2002). High proportions and abundances of A.

minitissimum were observed in association with extremely

high NO

2

+NO

3

concentrations in Yousheng Stream.

Correlation with environmental variables also showed that

the presence of A. minitissimum was positively correlated

with NO

2

+NO

3

concentrations in the streams. As a matter

of fact, A. minitissimum is known to have a high demand

for N (Fairchild et al., 1985; Carriok and Lowe, 1988) and

is considered to be a pollution-tolerant species in many

temperate streams (Krstic¡¦ et al., 1997; Kwandrans et al.,

1997; Soininen and Niemela, 2002). Correlation with

environmental variables also showed that Nostoc spp., D.

vulgaris, E. minutum, N. sinuate var. tabellaria, R. sinuate,

and S. ungeriana var. pseudogaillonii were positively

correlated with NO

2

+NO

3

concentrations. E. minutum

has been observed in areas with high and low nutrient

concentrations (Rier and Stevenson, 2006). In this study,

however, E. minutum was only observed in regions with

high NO

2

+NO

3

concentrations. These species might also

be considered to be N-tolerant taxa (Fairchild et al., 1985;

Rott et al., 1998; Winter and Duthie, 2000; Winter et al.,

2003).

TP was suggested as being an important factor

influencing the abundance and composition of diatoms in

streams (Soininen and Kononen, 2004). Todd et al. (1996)

found that phosphate enrichment increased the proportions

of smaller algae. In this study, TP concentrations were not

a primary factor structuring the epilithic algal communities

in the streams. However, the abundance of C. placentula

was found to be positively correlated with increased

TP concentrations. C. placentula is typical of meso- or

eutrophic taxon, and the optimum concentration of TP for

growth was 27-396

£ggL

-1

(Van Dam et al., 1994; Soininen

and Niemela, 2002; Kovacs et al., 2007). Although TP

concentrations did not differ significantly among any

regions, a clear seasonal pattern did emerge, especially

in summer and fall, when the discharge increased. At

that time, C. placentula replaced A. atomus and became

the most dominant species in this region. However, the

abundance of C. placentula quickly decreased in winter

when the discharge and TP concentrations in the stream

dropped.

Oscillatoria was frequently observed in streams with

high nutrient loading and slower current velocities.

Oscillatoria is also considered to be a pioneer taxon after

flooding (DeNicola and McIntire, 1990a; Stevenson,

1996). In the Wuling area, current velocity was slower

and NO

2

+NO

3

concentrations were higher in Yousheng

Stream. However, Oscillatoria was not the dominant

taxon in Yousheng Stream. Instead, Oscillatoria was

found to be more abundant in the lower reach of Cijiawan

Stream, especially in winter. The growth of Oscillatoria

has been found to be suppressed in high light conditions

(DeNicola and McIntire, 1990b). The removal of riparian

vegetation from Yousheng Stream might have increased

the amount of sunlight reaching the stream surface and

thus the water temperature. In the lower reach of Cijiawan

Stream, nevertheless, the higher riparian canopy and

NO

2

+NO

3

concentrations were more suitable for the

growth of Oscillatoria. This suggests that Oscillatoria is

not a sensitive bioindicator for monitoring agriculture in

tropical/subtropical streams.

In addition to the influence of agriculture, the

abundance of many diatoms was negatively correlated with

grazer density. Grazer density was also identified as one of

the major factors affecting spatial changes in epilithic algal

community. This suggests a top-down control of epilithic

algae by aquatic insects in the stream. Nevertheless,

Colletti et al. (1987) indicated that mayflies had little

effect on algal assemblages at an insect density of < 1000

individual m

-2

. In this study, the mean grazer density

was only 261-839 individual m

-2

(Table 1). However, a

higher proportion of caddisflies, a grazer, was observed

in the streams (Kuo and Chiu, 2005). The mouthparts of

caddisflies can scrape attached algae off hard surfaces

more effectively than the brush-like mouthparts of most

mayfly nymphs (Peterson et al., 1998; Holomuzki and

Biggs, 2006). This may be the reason that grazing effects

on the abundance of epilithic algae were detected in the

streams despite the low density of grazers. Grazing effects

on the community composition of epilithic algae need to

be further examined.

CONClUSIONS

The effects of agriculture on the subtropical streams

of the Wuling area were significant and varied with the

extent of agriculture in the catchment. The epilithic

YU and LIN ¡X Effects of agriculture on epilithic algae

85

algal communities were primarily affected by NO

2

+NO

3

concentrations in the streams resulting from agricultural

runoff. The epilithic algal biomass increased with

NO

2

+NO

3

concentration. Correlation analyses further

identified the cyanobacteria Nostoc spp. and the diatoms

A. minitissimum, A. atomus, D. vulgaris, E. minutum,

N. sinuata var. tabellaria, R. sinuate and S. ungeriana

var. pseudogaillonii as N-tolerant taxa. The diatoms

C. placentula, G. tergestinum var. tergestinum, and

Gomphonema sp.1 were more-closely related to increased

TP concentrations. Changes in abundance and community

structure of epilithic algae can be used to monitor the

effects of agriculture in tropical/subtropical mountain

streams.

Acknowledgements. This study was supported by the

Shei-Pa National Park Administration, Miaoli County,

Taiwan.

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