PRIMARY RESEARCH PAPER

Patterns of fish community composition along a riveraffected by agricultural and urban disturbancein south-central Chile

Rodrigo Orrego Æ S. Marshall Adams ÆRicardo Barra Æ Gustavo Chiang Æ Juan F. Gavilan

Received: 17 October 2006 / Revised: 2 September 2008 / Accepted: 18 September 2008 / Published online: 21 October 2008

� Springer Science+Business Media B.V. 2008

Abstract Patterns of fish community composition

in a south-central Chile river were investigated along

the altitudinal-spatial and environmental gradient and

as a function of anthropogenic factors. The spatial

pattern of fish communities in different biocoenotic

zones of the Chillan River is influenced by both

natural factors such a hydrologic features, habitat,

and feeding types, and also by water quality variables

which can reduce the diversity and abundance of

sensitive species. A principal component analysis

incorporating both water quality parameters and

biomarker responses of representative fish species

was used to evaluate the status of fish communities

along the spatial gradient of the stream. The

abundance and diversity of the fish community

changed from a low in the upper reaches where the

low pollution-tolerant species such as salmonid

dominated, to a reduced diversity in the lower

reaches of the river where tolerant browser species

such as cypriniformes dominated. Even though the

spatial pattern of fish community structure is similar

to that found for the Chilean Rivers, the structure of

these communities is highly influenced by human

disturbance, particularly along the lower reaches of

the river.

Keywords Fish � Assemblages � Sewage �Cause–effect relationship

Introduction

Fish community composition along the spatial gradi-

ent of streams and rivers is influenced by both natural

factors and anthropogenic stressors (Vannote et al.,

1980; Aarts & Nienhuis, 2003). Under natural

conditions, a river is characterized by either a

continuous succession of fish species along the

spatial gradient (Illies & Botosaneanu, 1963; Schw-

oerbel, 1983) or a staggered succession, where, for

example, a fluvial system can be defined as a function

of gradient, current velocity, and temperature which

highly influence the community composition (Huet,

1954; Campos, 1985). Along the downstream gradi-

ent the River Continuum Concept (Vannote et al.,

Handling editor: C. Sturmbauer

R. Orrego � R. Barra � G. Chiang

Aquatic Systems Research Unit, Environmental Science

Center EULA-Chile, University of Concepcion,

Concepcion, Chile

R. Orrego (&)

University of Ontario Institute of Technology, 2000

Simcoe Street North, Oshawa, ON, Canada L1H 7K4

e-mail: Rodrigo.Orrego@uoit.ca

S. Marshall Adams

Environmental Sciences Division, Oak Ridge National

Laboratory, Oak Ridge, TN, USA

J. F. Gavilan

Department of Cellular Biology, Faculty of Biological

Sciences, University of Concepcion, Concepcion, Chile

123

Hydrobiologia (2009) 620:35–46

DOI 10.1007/s10750-008-9613-8

1980) relates community structure and river func-

tional changes, with physical factors such as flow

regime, temperature, food availability, and river

morphological conditions. This concept suggests that

the physical aspects of the stream are relatively stable

which are responsible for the consistent pattern in

biological community structure. Schloseer (1982)

established that fish community structure and river

functional changes support the qualitative basis of the

stream continuum concept within the range of

available of resources such as habitat and food.

Fish community composition and associated spa-

tial and temporal changes can also be defined by

species richness and trophic patterns (Oberdorff

et al., 1993) or by eco-region classification based

on stream thermal regime (Lyons, 1996), both species

richness and trophic patterns are also influenced

anthropogenic disturbances along temporal and spa-

tial gradient and they require large data sets to

establish possible causal relationships with human

disturbances. In addition, the patterns of fish com-

munity structure in lotic systems can be influenced by

other biological factors (such as competition and

predation), physicochemical factors such as water

flow, channel morphology, habitat (Capone &

Kushlan, 1991; Jackson et al., 2001), and point and

non-point pollution sources (Dauba et al., 1997;

Ibarra et al., 2005). The influence of non-point source

pollution on fish community structure is controversial

and difficult to evaluate (Ibarra et al., 2005), espe-

cially due to the low probability for establishing

definitive causal relationships. Both natural and

anthropogenic factors can affect habitat stability of

fish communities (Alay et al., 1995), altering the

normal structural and functional dynamics of fish

communities along a spatial gradient.

Freshwater fish communities in Chile are repre-

sented by a richness of 46 native species (Campos

et al., 1993) resulting in a high endemism (species

only found in Chilean rivers), not only at the species

but also at the gender and family levels (Arratia et al.,

1981; Campos et al., 1993; Ruiz et al., 1993).

Maintaining such a high level of endemism requires

relatively high natural habitat stability along spatial

and temporal gradients of lotic systems (Campos,

1970; Arratia et al., 1981; Gavilan, 1992; Campos

et al., 1998). The watersheds of most river systems in

south-central Chile are characterized by permanent

snow fields in the higher elevations, native forests in

the middle and lower areas, and some bare rock and

grasslands habitats interposed between the upper and

lower areas. Although still restricted in extension,

exotic species forestry plantations (Eucalyptus and

Pinus spp.) have been intensely introduced in the

south-central Chile in the last decades. Land use in

the Central Valley is mainly agricultural, with

predominance of sugar beet, wheat, and pastures

particularly in the Chillan River watershed. In

addition to these natural and land use factors, an

important untreated sewage discharge has a major

influence of the water quality of the lower Chillan

River (Cooman et al., 2005; Debels et al., 2005).

The specificity and simplicity of biomarkers are

especially useful to help establish possible causal

relationships between biological effects and water

quality caused by pollution, two biomarkers were

measured in a representative fish species. Biomarkers

are sensitive and rapidly responding indicators of

toxicant exposure (Adams, 2002).

The objectives of this study are to describe the

spatial and temporal pattern distribution of fish

communities in the Chillan River and to determine

the relationship, using a multivariate statistical

approach, between fish community composition and

influential natural and anthropogenic environmental

factors. Such information is valuable for responsible

environmental management and conservation of

native fish communities.

Materials and methods

Study area

The Chillan River is characterized as a tertiary-order

short river, corresponding to a Rhithral environment

with a high gradient and water velocity, which is

typical for many Andean rivers in southern Chile

(Illies & Botosaneanu, 1963; Campos, 1985). This

river can be segregated into three Biocoenotic zones

based on physical habitat characterization (Illies &

Botosaneanu, 1963), a high gradient river zone (Epir-

ithron) dominated by rapids with high water velocity, a

middle zone (Metarithron) alternating between rapids

and pools, and a lower zone (Hyporithron) with a

gradual gradient, characterized by extensive pool

areas and reduced water velocity. The watershed is

located in south-central Chile (36�330–36�530 S;

36 Hydrobiologia (2009) 620:35–46

123

72�210–71�240 W) and contains a total drainage area of

ca. 757 km2, with 27% of the watershed located in the

Andes Mountain and 73% situated in the Chilean

Central Valley (Fig. 1). Altitude in the watershed

ranges from 3,200 m in the upper part to 75 m at the

river outlet. The total length of the River from its

headwaters to its confluence with the Nuble River is

105 km. The mean annual flow of the Chillan River is

22.9 m3 s-1; however, flow rates can drop below

1 m3 s-1 during the dry season due to irrigation and

drinking water withdrawals. One of the main factors

affecting water quality is an untreated sewage dis-

charge located downstream of the city of Chillan

(Fig. 1).

Fish community sampling

Spatial structure of fish communities in the Chillan

River were investigated by collecting fish at five sites

along a spatial gradient (S1–S5) and at three sites (S6,

S7, S8) in the main tributaries (Fig. 1). Temporal

variations in fish communities were assessed by

conducting four samplings over a 16-month period.

This survey was conducted during two Chilean

austral summer periods (January 2000 and February

2001) and two spring periods (November 1999 and

November 2000). Water quality parameters including

temperature, pH, conductivity, dissolved oxygen,

Biochemical Oxygen Demand (BOD), suspended

solids, total nitrogen, and total phosphorus (Debels

et al., 2005) and fecal coliforms (Cooman et al.,

2005) were measured at all sites during each

sampling period as a component of the Watershed

monitoring program (EULA-Chile, 2002). Water

quality information was used to determine multivar-

iate statistic relationships with the spatial and

temporal patterns of fish community composition.

Fish were sampled using backpack electrofishing

techniques (Elektrofishfangerat motor JLO gasoline)

and the sampling effort at each site was standardized

based on equal sampling times and similar area cover.

Captured fish were on site identified to species level

and weight and standard length recorded. For

biomarkers analysis, a few individuals of the most

common species were sacrificed and tissue sampled

(all other fish species were returned to the river in the

same area). The condition factor K was calculated as

(total weight 9 100/total length3). Fish community

parameters were calculated for each sample site,

including relative abundance of each species, the

Shannon Diversity index (H0), and the Maximum

Diversity (Hmax) and Equity (J0) indexes (Saiz, 1980;

Lambshead et al., 1983).

Biomarkers

Two selected biomarkers were analyzed in represen-

tative fish species (Trichomycterus areolatus), which

occurred at each biocoenotic areas and sampling

times. Acetylcholinesterase (AChE) inhibition eval-

uation, which is a classical biological endpoint used

to assess fish exposure to certain organophosphate

and carbamate insecticides, was included (Sandahl

et al., 2005). AChE, the regulation cholinergic

signaling enzyme by hydrolyzing the transmitter

acetylcholine at central and peripheral synapses in

the vertebrate nervous system can be inhibited by

both organophosphate and carbamate insecticides

(widely used in Chilean agricultural activities).

Additionally, the Cytochrome P450-dependent MFO

system observations were included in the final

analysis. CYP1A1 are the principal enzymes cata-

lyzing oxidative metabolism of toxicants. Measured

as hepatic microsomal ethoxyresorufin-O-deethylase

(EROD) activity induction is another reliable and

widely used biomarker of organic pollutants exposure

in fish (Whyte et al., 2000).

Fig. 1 Study area of the Chillan River Basin, south-central

Chile. Sampling sites are S1 (Esperanza), S2 (Pte. Pinto), S3

(ESSBIO), S4 (Pte. Nebuco), S5 (Vista Bella), S6 (Boyen), S7

(Lajuelas) and S8 (Quilmo). (Arrow indicates the Chillan City

sewage discharge)

Hydrobiologia (2009) 620:35–46 37

123

A total of 10 individuals at each site (size range

3.5–4.5 cm) were brain and liver tissue sampled, and

stored in liquid nitrogen until analysis.

Brain tissue from each fish was homogenized in a

1:15 (w/v) ratio with 0.1% Triton X-100 in Tris/HCl

(25 mM, pH 8.0) and the enzymatic activities deter-

mined by the spectrophotometric method (Ellman

et al., 1961) using acetylthiocholine iodide as substrate

and the increase in absorbance at 410 nm was recorded

(5 min) using a lambda 2 (ultraviolet-visible) spectro-

photometer (PerkinElmer). Enzymatic activity was

expressed as mol/min/mg protein (protein analysis was

performed using a Bio-Rad Protein Kit). Cytochrome

P450 enzyme (CYP1A1) activity was evaluated as

EROD (Lubert et al., 1985) in the post-mitochondria

(fraction S9) obtained from livers homogenized in a

sucrose buffer using an LS 50B spectrolfluorimeter

(PerkinElmer, Beaconfield, UK) for 5 min at 25�C and

value expressed as pmol/min/mg protein.

Statistical analysis

A similarity index based on the Bray-Curtis and

Multimetric Cluster Analysis were used to describe

differences in fish community structure among tem-

poral and spatial gradients of the Chillan River.

Physico-chemical and biological variables were log-

transformed to avoid non-normality, and then stan-

dardized with a mean of Zero and standard deviation

of one (Field et al., 1982). A multivariate Principal

Component Analysis (PCA) with varimax rotation

was conducted in order to identify structure in the

relationships between all measured variables and to

reduce the number of variables included, identifying

which factors were most responsible for the observed

variance (Data analysis software system: STATISTI-

CA 7.1, Copyright�StatSoft, Inc. 2005).

Results

Distribution patterns and community structure

A total of 15 fish species representing 12 families

were identified in the Chillan River (Table 1). Ten

species are native of Central Chile and categorized as

vulnerable or in danger of extinction. The dominant

fish species in the upper section of the Chillan River

(S1) during all sampling times was O. mykiss, an

introduced species which was captured only at this

site, and T. areolatus was the most widely distributed

native species captured along the entire apatial

gradient of the river (S1, S2, S3, S5, S6, and S7).

In the middle zone (sites S2 and S3) including the

area of the sewage discharge (between sites S7 and

S8), the dominant native species were T. areolatus,

P. trucha, and P. irwini. In the lower reach of the

river (sites S4 and S5), dominant species were Ch.

galusdae (native) and C. carpio (introduced) which

were present only at S5. Distribution of these species

along the spatial gradient of the stream is shown in

Fig. 2.

Along the spatial gradient of the stream the

condition factor (K) did not vary for the majority of

the species except for representatives of the Characi-

dae, Perciliidae, Percichthyidae, and Salmonidae

families (Table 3). Some differences in the condition

factor (K) were observed in the fish from the

Trichomycteridae, Atherinopsidae, Galaxiidae, and

Geotriidae families due to their typical halometric

growth (disproportional growth in length compared to

weight; Campos et al., 1993).

The level of spatial coexistence among species

was evaluated using the abundance percentage of

each species at each site. This information was

generated using similarity indexes such as the Bray-

Curtis Index represented by Cluster Analysis dend-

ograms (Biodiversity Professional Beta 1 Program).

The fish community similarity analysis indicate a

large difference for site between the upper and lower

sections of the river with a high similarity from the

middle section of the river (S2 and S3) and decreas-

ing to the lower section of the river (S5) during the

first sampling period (Fig. 3). The second sampling

period results (January 2000) demonstrate the exis-

tence of two similar community groups; a large group

that includes the fish communities of S6 and S7 (the

principal tributary) and S2 and S3 (middle zone of the

river). A second distinct group includes the fish

communities present in S4 and S8 (lower reaches of

the river). Results of the third sampling time

(November 2000) indicated a similarity group that

comprises the fish communities of the middle river

(S2, S3, and S7) with similarity diminishing at the

lower river site (S4). Differences in community

similarity between the upper and lower sites are

greater than that between the middle and lower

reaches. Results from the fourth sampling period

38 Hydrobiologia (2009) 620:35–46

123

Ta

ble

1P

rin

cip

alch

arac

teri

stic

so

fth

eC

hil

lan

Riv

erfi

shco

mm

un

ity

Fam

ily

Sp

ecie

sn

Sp

ecie

s

typ

e

Cat

ego

rya

Do

min

ant

(sta

tio

ns)

%A

bu

nd

ance

No

vem

ber

19

99

Jan

uar

y

20

00

No

vem

ber

20

00

Feb

ruar

y

20

01

(S1

)(S

2,

S3

)(S

4,

S5

)

Ath

erin

op

sid

aeB

asi

lich

thys

au

stra

lis

12

01

9N

V–

–5

.28

–

Ch

arac

ide

Ch

eiro

do

ng

alu

sda

e3

61

12

21

8N

V(S

4,

S5

)–

5.0

41

6

Cy

pri

nid

aeC

ypry

nu

sca

rpio

8–

–2

I–

(S5

)–

–7

Dip

lom

yst

idae

Dip

lom

yste

sn

ah

uel

bu

taen

sis

1–

––

NE

D–

0.6

3–

–

Gal

axii

dae

Ga

laxi

am

acu

latu

s–

––

1N

V–

––

2

Geo

trii

dae

Geo

tria

Au

stra

lis

33

––

NV

––

0.9

6–

Icta

luri

dae

Am

eriu

rus

mel

as

–1

4–

–I

––

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.16

–

Per

cich

thy

idae

Per

cich

thys

tru

cha

28

84

20

30

NV

(S2

,S

3),

(S4

,S

5)

–2

42

4

Per

cili

idae

Per

cili

air

win

i3

5–

41

12

NE

D(S

2,

S3

),

(S4

,S

5)

5.3

71

64

3

Po

ecil

iid

aeG

am

bu

sia

affi

nis

––

–1

9I

––

––

3.3

Sal

mo

nid

aeO

nco

rhyn

chu

sm

ykis

s8

21

41

5I

–(S

1)

52

––

Sa

lmo

tru

tta

16

31

4I

–(S

1)

17

4.0

8–

Tri

cho

my

cter

idae

Tri

cho

myc

teru

sa

reo

latu

s6

13

23

31

00

NV

(S1

), (S2

,S

3)

25

36

4.7

Nem

ato

gen

ysin

erm

is5

––

–N

ED

––

0.7

2–

Bu

llo

ckia

ma

ldo

na

do

i8

2–

24

NE

D–

–5

.76

–

NN

ativ

e,I

intr

od

uce

d,

Vv

uln

erab

le,

ED

exti

nct

ion

dan

ger

aC

amp

os

etal

.(1

99

8)

Hydrobiologia (2009) 620:35–46 39

123

(February 2001) demonstrates a high similarity

between the fish communities from the middle river

zone (S2 and S3) which are marginally different from

the upper and lower reaches.

The specific diversity (H0), maximum diversity

(Hmax), and equity (J0) analysis of the first three

sampling periods indicate a high diversity (H0) in the

fish communities present in the middle reach (S2 and

S3) compared to the upper and lower reaches sites.

The maximum diversity in all the sampling periods

was observed located in the middle river section (S2

and S3) (Table 2).

Biological characterization

Fish community diversity in each of the three

biocoenotic zones of the river was also characterized

by the relative feeding types and also by the number

of tolerant and intolerant pollution species (Table 3).

In the upper Epirithron zone (zone 1), pollution

intolerant species such as salmonids (O. mykiss)

dominated and contributed over 50% of the relative

abundance of fish species present, even though this

species does not occur in the other two zones.

Because this species comprises such as large com-

ponent of the fish community in zone 1, diversity is

relatively low in the upper reaches of the river. In the

middle section or Metarithron zone (zone 2),

T. areolatus, which is an omnivorous and an inter-

mediate pollutant tolerant species, dominates the fish

community where community diversity is relatively

high (Table 1). Pollutant tolerant species that are

primarily omnivorous or benthic detrivores such as

Gambusia affinis and C. carpio, respectively (both

introduced), appears only in the lower section or

Hyporithron zone (zone 3). These pollution tolerant

species were not found in the upper two biocoenotic

zones and are commonly associated with slow

flowing and degraded quality water conditions

(Campos, 1970; Campos et al., 1993, 1998).

Fig. 2 Altitudinal spatial

gradient of the Chillan

River fish community for

each site and sampling

period. Black dots represent

the presence of the

particular fish species

collected at that site and

time

40 Hydrobiologia (2009) 620:35–46

123

Physicochemical characterization

In addition to the spatial gradient in habitat types

along the river, there is a gradient in physicochemical

parameters primarily caused by organic discharges

into the system (Table 4). Basic physicochemical

parameters such temperature and conductivity

increased, while dissolved oxygen decreased from

the up-river sections to the lower reaches (eutrophic

hyporithron). Parameters related to the organic load-

ing from the sewage discharge including total

nitrogen, fecal coliforms, total phosphorus, and

suspended solids were significantly higher in the

lower reaches (hyporithron biocoenotic zone) during

the four sampling periods. Consequently the water

quality index in this zone was reduced by almost 45%

(WQI; Debels et al., 2005). Also, a significant

increment in coliforms was observed in this zone

(Cooman et al., 2005).

Biomarkers

No significant decrease in brain AChE enzymatic

activities of the representative species T. areolatus

were observed among the biocoenotic areas and

sampling periods (Fig. 4A). However, significant

induction of the liver EROD enzymatic activity of

these fish was observed (Fig. 4B) during all four

sampling periods. A 3-fold and 6-fold increase in

EROD activity were observed in fish from the mid

and lower zones of the river, respectively (meta and

hyporithron), compared to those from the upper zone

(epirithron).

Fig. 3 Bray-Curtis similarity analysis among the sampling

sites and collection periods

Table 2 Shannon index (H0), maximum diversity (Hmax), and

equity (J0) of the Chillan river fish community during the four

sampling periods

Sites H0 Hmax J0

November 1999 S1 0.581 0.699 0.832

S2 0.715 0.903 0.792

S3 0.72 0.903 0.797

S5 0.636 0.699 0.91

January 2000 S2 0.439 0.477 0.921

S3 0.505 0.602 0.838

S6 0.566 0.699 0.81

S7 0.482 0.845 0.571

S8 0.323 0.477 0.677

S4 0.297 0.301 0.985

November 2000 S1 0.284 0.477 0.596

S2 0.407 0.477 0.853

S3 0.565 0.602 0.939

S7 0.518 0.699 0.742

S4 0.141 0.301 0.469

February 2001 S1 0.484 0.602 0.803

S2 0.477 0.477 1

S3 0.487 0.778 0.626

S8 0.392 0.602 0.651

S4 0.506 0.602 0.841

S5 0.581 0.778 0.746

Hydrobiologia (2009) 620:35–46 41

123

Multivariate statistical analyses

In order to identify whether biological and physico-

chemical parameters measured are correlated and

which of these are responsible for most of the spatial

and temporal variance observed, a Principal Compo-

nent Analysis (PCA) was conducted. Due to the

skewness in sample data distribution, this analysis

was performed using log-transformed data. The result

of the PCA analysis (Table 5) indicated that PCA-

Factor 1 explains 44.7% of the total variance

observed and is highly influenced by parameters

such as nitrates, phosphates, coliforms, conductivity,

and COD which are directly related with the input of

Table 4 Physicochemical, characterization of the three biocoenotic zones in the Chillan River watershed (EULA-Chile, 2002)

ZONE 1

Epirithron

ZONE 2

Metarithron

ZONE 3

Hyporithron

Coliforms MPN/100 ml 2.5 (1.1) 8.3 (4.4) 18175.1 (9863.2)

Total phosphorous mg/l 0.011 (0.003) 0.025 (0.003) 0.493 (0.951)

Total nitrogen mg/l 0.062 (0.004) 0.153 (0.086) 1.259 (0.721)

Suspended solids mg/l 7.825 (0.546) 9.65 (1.76) 12.913 (7.464)

BOD mg/l 1.675 (0.472) 1.487 (0.627) 4.125 (2.551)

Conductivity lS/cm 57.85 (27.40) 59.06 (26.23) 153.04 (78,11)

pH – 7.425 (0.579) 7.587 (0.786) 7.525 (0.765)

Temperature �C 10.91 (3.16) 13.60 (1.66) 17.22 (2.75)

Dissolved oxygen mg/l 9.01 (0.22) 8.0 (0.17) 4.6 (2.63)

WQIa % 97 (1) 84 (6) 59 (13)

a Debels et al. (2005)

Table 3 Biological characterization of the three biocoenotic zones in the Chillan River watershed

Mayor species

present

Relative

abundance (%)

Diversity (H0) Condition

factor (K)

Feeding typesa Pollution

tolerance

level

Zone 1 Epirithron O. mykiss 52 0.59 ± 0.11 0.98 ± 0.11 Fish/Crustacean/

Insect

Lowb

T. areolatus 25 0.90 ± 0.09 Insect larva/

Amphypod

Mediumc

S. trutta (other two

species)

17 1.23 ± 0.27 Fish/Crustacean/

Insect

Lowb

6

Zone 2 Metarithron T. areolatus 36 0.761 ± 0.15 0.89 ± 0.12 Insect larva/

Amphypod

Mediumc

P. trucha 24 1.44 ± 0.28 Crustacean/

Amphipods

Mediumc

P. irwini (other seven

species)

16 1.47 ± 0.16 Insect/

Crustacean

Mediumc

24

Zone 3 Hyporithron P. irwini 43 0.734 ± 0.05 1.45 ± 0.07 Insect/

Crustacean

Mediumc

Ch. galusdae 16 1.46 ± 0.09 Alga/Insect Highc

P. trucha 24 1.36 ± 0.17 Crustacean/

Amphipods

Mediumc

C. carpio (other three

species)

7 1.02 ± 0.08 Alga/(browse

species)

Highc

10

a Campos et al. (1993); b Campos (1970); c Campos et al. (1998)

42 Hydrobiologia (2009) 620:35–46

123

a point source (sewage discharge). The first PCA-

Factor is also influenced by the fish biochemical

biomarker responses to the organic compounds

exposure (induction EROD activity) and the commu-

nity parameters Hmax and H. The bi-dimensional

space distribution of the PCA Factor 1 and Factor 2

(explaining an additional 15.8%) also indicate a

cluster of parameters such as nutrients, molecular

biomarkers, and community indexes (Fig. 5A) being

important for explaining spatial and temporal trends

in the data. A similar result was observed using PCA-

Factors 1 and 3, where the clustering of parameters

was even tighter (Fig. 5B). Both bi-dimensional

distribution graphs identify an isolated water quality

index WQI more associated with the AChE activity

which is used to indicate pesticide exposure (diffuse

source in the watershed).

Discussion

Fish are not homogenously distributed along the

spatial gradient of lotic systems but are highly

influenced by the physicochemical and biotic

conditions along this gradient (Aarts & Nienhuis,

2003). Identifying ecological units within lotic sys-

tems is relatively difficult because of the importance of

both biotic and abiotic factors in influencing the nature

of fish communities. For southern Chilean Andean

Rivers, Campos (1985) emphasized the relationship

between these biotic and abiotic factors in shaping

zonation of fish communities. Our initial description of

the Chillan River was based on the classification

criteria of Illies & Botosaneanu (1963); however, our

results are more consistent with those of Durrchmidt

(1980) and Hynes (1970) who argue that classification

categories of biocoenotic areas are valid only in a

general sense for the Andean rivers of Chile. Typical

zonation of fish in the Chillan river consists of an upper

zone (S1) characterized by dominance of an intro-

duced species (O. mykiss), a middle zone (S2 and S3)

characterized by an increased diversity where P. trucha

and P. irwini species dominates, and a lower zone

where diversity is reduced and characterized by

P. irwini, Ch. galusdae, and C. carpio species.

Results of fish community-related studies con-

ducted in other south Chilean rivers found similar

Table 5 Result of the principal component analysis (bold

values [0.70)

Factor 1 Factor 2 Factor 3

Eigenvalues 7.15 2.53 1.98

% Variance 44.68 15.81 12.36

Accumulative % 44.68 60.49 72.85

Factor loadings (varimax normalized)

H 0.84 0.25 -0.21

Hmax 0.75 0.07 0.15

J 0.36 0.35 -0.67

CF 0.88 -0.34 -0.02

Cond 0.73 0.49 0.34

BOD 0.40 20.76 0.30

COD 0.77 -0.40 0.31

Phosp 0.88 -0.06 0.24

Nitr 0.93 -0.25 0.03

pH 0.55 0.77 0.23

SS 0.51 -0.18 -0.50

Temp 0.76 0.48 0.12

WQI -0.31 0.47 0.51

DOx 0.01 -0.03 0.53

AChE -0.26 -0.27 0.43

EROD 0.86 -0.19 -0.24

Fig. 4 Biomarker analysis of T. areolatus in the Chillan River.

A Brain AChE activity; B Liver EROD activity. *Significant

difference (analysis of variance. P \ 0.05; confirmed by Tukey

post hoc test, P \ 0.05)

Hydrobiologia (2009) 620:35–46 43

123

spatial patterns in number of native species and the

ratio between native and introduced species (Campos,

1973; Arratia et al., 1981; Habit, 1994; Ruiz & Berra,

1994). However, these previous studies did not

investigate patterns of spatial and temporal zonation

of fish communities as a function of influential

environmental factors including those associated with

human disturbance. Recently studies (Habit et al.,

2005) documented dramatic changes during the last

decade in the fish communities in the middle section

of the Biobio River such a rapid shift in fish

community zonation attributed to increases in human

activities along the watershed including sewage and

pulp mill discharges; however, no cause–effects

relationships were demonstrated.

Fish community stability can be highly affected by

point and non-point sources of pollution associated

with land use (Ibarra et al., 2005), and in the case of

Andean rivers in Chile, most land use activities

involve agricultural and urbanization of watersheds.

Anthropogenic disturbances such as inputs of con-

taminants and nutrients, heavy loading of silt and

suspended matter, and episodic temperature regimes

can destabilized systems resulting in decreases in the

diversity and abundance of biological communities

(Death & Winterbourn, 1995). This situation appears

to be the case in the Chillan River where anthropo-

genic disturbance has destabilized the system

resulting in fish communities that are characteristic

of stressed aquatic ecosystems.

There is no common consensus regarding the

relative importance of natural versus anthropogenic

factors in determining the fish assemblages and

communities along spatial and temporal scales

(Jackson et al., 2001). Using a multivariate analysis

approach that includes both natural and anthropo-

genic factors provided an opportunity to test our

hypothesis regarding the spatial assemblage of the

Chillan River fish community. Although, no index or

model can adequately explain cause–effects relation-

ship based only on physicochemical and biological

observations and correlations, the emphasis of our

analysis was to investigate the fish assemblage

composition as a function of influential environmen-

tal variables along the spatial gradient of the stream.

This study demonstrated that there were significant

relationships among all the parameters that were

highly influenced by the Chillan city sewage dis-

charge (Fecal Coliforms, Phosphorus, Nitrogen,

COD, Conductivity, and Temperature). These dis-

charges not only caused significant biomarkers

responses (EROD activity) in fish but also altered

the fish community index as Shannon Diversity index

(H0) and Maximum Diversity (Hmax).

The observed pattern of fish communities in the

Chillan River was clearly influenced by the anthropo-

genic disturbances caused by discharges of untreated

sewage effluent into the river, suggesting a cumulative

spatial effect due to nutrient enrichment (eutrophica-

tion) which resulted in habitat loss and environmental

degradation in the lower reaches of the river. Results

of toxicity studies and water quality assessment

Fig. 5 Principal Component Analysis (PCA). Bi-dimensional

spatial distribution (varimax rotation). A Spatial distribution of

Factor 1 and Factor 2, and B spatial distribution of Factors 1

and 3. WQI: Water Quality Index, AChE: Acetylcholinester-

ase, DOx: Dissolved Oxygen, BOD: Biochemical Oxygen

Demand, Cond: Conductivity, COD: Chemical Oxygen

Demand, Phosp: Phosphorous, Hmax: Maximum Diversity,

Temp: Temperature, Cf: Fecal coliforms, Nitr: Total Nitrogen,

H: Shannon Diversity index, EROD: ethoxyresorufin-O-

deethylase, Ss: suspended solids, J: Equity index

44 Hydrobiologia (2009) 620:35–46

123

conducted simultaneously in this river also found an

increase in acute and chronic effects in Daphnia

toxicity test with surface waters and a decrease of the

water quality index (WQI) downstream of the Chillan

city sewage discharges (Cooman et al., 2005; Debels

et al., 2005). However, combining these parameters

with fish community and molecular biomarker infor-

mation in a multivariate analysis indicated that the

water quality index (based primarily on dissolved

oxygen or COD) does not appear to be related with the

composition of the fish community.

Conclusion

The Chillan River in south-central Chile is a classical

example of how environmental perturbations from

anthropogenic stressors can destabilize and disrupt

the normal pattern of spatial zonation of fish

communities and their controlling biotic factors.

Although the pattern of fish assemblage composition

in the Chillan River follows those typically described

for Chilean Rivers, such patterns are highly influ-

enced by sewage discharges and the resulting nutrient

enrichment (eutrophication) and organic pollution.

This spatial pattern in species abundance, diversity,

and occurrence is related to the organic loading of the

river that was confirmed by establishing causality

using the biomarkers assessment.

When evaluating the impact of human disturbance

on the structure and composition of fish communities,

assessing the temporal state of biocoenotic zones in

aquatic systems and in combination with identifica-

tion of causal variables, appears to be a suitable

strategy that provides important information that can

be used to improve environmental management and

regulation of aquatic ecosystems, particularly where

threatened and endangered species are involved.

Acknowledgments This work was partially financed by the

Chilean Agricultural and Livestock Service (Servicio Agrıcola

y Ganadero (SAG) de Chile Fondo SAG No. VIII 4-36-0199)

and by the Project P.I. No. 202.031.090-1.0 of the Research

Directorate of the Universidad de Concepcion, Chile.

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