Microhabitat use by fish in the upper Rio Matarraña, Spain, 1984–1987

Eco/ogy of Freshwater Fish 1994: 3; 141-152 Printed in Denmark . All rights reserved

Copyrinhl 8 Munksxaard 1994

ECOLOGY OF FRESHWATER FISH

ISSN 0906-6691

Microhabitat use bv J

fish in the Matarrafia, Spain, -1984-1987

Grossman GD, de Sostoa A. Microhabitat use by fish in the upper Rio Matarrafia, Spain, 1984-1987. Ecology of Freshwater Fish 1994: 3: 141-152. 0 Munksgaard, 1994

Abstract - We evaluated the microhabitat use and abundance of Barbus graellsii, Bardus haasi, Chondrostoma toxostoma, Noemacheilus barbatulus, Oncorhynchus mykiss and Rutilus arcasii between 1984 and 1987 in the upper Rio Matarrafia, Spain. The mean abundance classes for all species ranged from 1.8 to 3.0 (where 1=1-6, 2=6-10, 3=11-20 and 4=>20 specimens, respectively). Mean abundance was consistently higher in 1984-1985 (2.4-3.0) than during 1986-1987 (1.8-2.8). The decreases noted in 1986-1987 were attributable to declines in abundance of 0. mykiss (introduced in winter 1984) and B. haasi. Barbus graellsii and Ch. toxostoma, however, remained abundant throughout the entire 4-year study. We only observed N. barbatulus and R. arcasii irregularly in the study site. Analyses of microhabitat availability data indicated that the study site contained more silt and less algae/debris during spring 1985 and early and late summer 1986 than in the majority of the remaining season. The converse was true for late summer 1985 (i.e., less silt and more algaeidebris than the majority of seasons). Principal component analyses showed that B. graellsii and Ch. toxostoma generally occupied deeper microhabitats with low to average velocities, higher amounts of depositional substrata and lower quantities of erosional substrata. B. haasi tended to avoid microhabitats with rubble substrata and occurred in those with higher amounts of algae/debris. 0. mykiss occupied shallower areas with slightly higher velocities and a heterogeneous substratum. With the exception of B. haasi, microhabitat use by assemblage members was similar from 1984 to 1987. B. haasi, however, was not as strongly affected by depth in the latter two years of the study as it was during 1984-1985. Seasonal and annual analyses of intraspecific microhabitat use showed that most changes were due to variations in microhabitat availability. Nonetheless, all species exhibited minor seasonal shifts in microhabitat use. Size-related analyses indicated that both smaller B. graellsii and Ch. toxostoma occupied shallower microhabitats with slower velocities than larger specimens. Intersite differences in microhabitat use for B. graellsii and Ch. toxostoma showed that most differences in substratum use were attributable to disparities in substratum availability. Both species occurred closer to the substratum in the site with higher velocities (i.e., upper reach), although this response was more pronounced in Ch. toxostoma. Interspe- cific analyses indicated that B. graellsii and Ch. toxostoma did not consistently occupy statistically differentiable microhabitats, although both species occurred farther from the substratum and refuges than did B. haasi. 0. mykiss occupied shallower microhabitats with more gravel than either B. graellsii or Ch. toxostoma. The lack of microhabitat shifts by native species during the study period indicates that interactions with either B. haasi or 0. mykiss did not play a strong role in microhabitat use by the remaining assemblage members.

Rio

G. D. Grossman1~2, A. de S0st0a3 'Warnell School of Forest Resources, University of Georgia, Athens, USA, 3Departamento de Biologia Animal (Vertebrados), Facultad de Biologia, Universidad de Barcelona, Spain

Key words: microhabitat use; spatial resource partitioning; competition; assemblage organization; cyprinidae; stream fish Gary 0. Grossman, Warnell School of Forest Resources, University of Georgia, Athens, GA 30602, USA Accepted for publication September 14, 1994

Un resumen en espaiiol se incluye detras del texto principal de este articula

141

Grossman & de Sostoa

Introduction

This article and its companion (Grossman & de Sostoa 1994) summarize a 4-year study of microhabitat use by fishes in the Rio Matarraiia, Spain. The site examined herein, however, is representa- tive of the upper reaches of the river and is similar to what has been termed the barbel zone by Huet (1949). It has higher velocities, lower temperatures and a more heterogeneous substratum than the lower Matarrafia (Grossman el al. 1987a, b). In addition, this site possesses greater physiognomic stability and is less influenced by seasonal environmental variations than the lower Matarrafia (Grossman et al. 1987a, b).

The fish assemblage of the upper Matarraiia, like many European rivers, is dominated by cypri- nids (Grossman et al. 1987b). During late autumn 1984, however, a local government agency acciden- tally introduced approximately 20 age 1 + rainbow trout (Oncorhynchus mykiss, formerly Salmo gaird- neri) into the study site. The introduction of this exotic species enabled us to test for the presence of interspecific competition for space in this assemblage. Consequently, we examined the following questions in the upper Matarrafia: 1) do fishes exhibit nonrandom microhabitat use? 2) do assemblage members exhibit seasonal or size-related variations in microhabitat use? 3) do Barbus graellsii and Chondrostoma toxostoma display similar patterns of microhabitat use in both upper and lower reaches? and 4) are patterns of microhabitat use by assemblage members suggestive of interspecific competition or species-specific responses to varying environmental parameters?

Material and methods

Because the species, study site, field and statistical methods, are described in Grossman et al. (1987a, b), we do not characterize them in great detail. In

brief, microhabitat observations were made during 14 sampling periods between 1984 and 1987. Sam- pling dates and seasonal assignations are as follows: early summer 1984 (25-27 June), late summer 1984 (17-18 August), winter 1984 (19-20 De- cember), spring 1985 (30 April, 1-2 May), late summer 1985 (9-10, 12 August), autumn 1985 (2- 3 November), winter 1985 (18-19 January), spring 1986 (23-25 March), early summer 1986 (28-29 May), late summer 1986 (1617 July), autumn 1986 (9 November), spring 1987 (27-28 March), early summer 1987 (20-30 May), autumn 1987 (26-27 November) .

To examine nonrandom microhabitat use, we made underwater observations of fishes and ana- lyzed these data using the principal component technique (PCA) of Grossman & Freeman (1987). We tested for intersite differences in microhabitat use by comparing the utilization patterns of B. graellsii and Ch. toxostoma in both sites using ca- nonical analysis of discriminants (CAD). These comparisons were made on a seasonal basis to control for changes in microhabitat availability. We eliminated distance from refuge from analyses, because the refuge structure of the two reaches differed substantially (i.e., Cladophora mats versus boulders and undercut banks). In addition, because the sites also differed in mean depth, we di- vided distance from the substratum of a specimen by total depth, to derive a relative depth for each fish. This measure is the most appropriate metric for intersite comparisons of depth utilization (Moyle & Senanayake 1984).

To test for microhabitat shifts caused by the presence of 0. mykiss, we compared habitat use patterns of assemblage members when 0. mykiss was both present (i.e., winter 1984-early summer 1986) and absent (i-e., early and late summer 1984, autumn 1986-autumn 1987). If competition for space occurred between 0. mykiss and other assemblage members, then microhabitat use should

Table 1. Mean abundance for upper Matarraiia fishes. Abundance classes are: 0=0 individuals observed, 1 =1-5 individuals observed, 2=6-10 individuals observed, 3=11-20 individuals observed, 4 = S O individuals observed. There was no variation among abundance estimates made on successive days.

Early Late Early Late Spring summer summer Autumn Spring summer summer Autumn

Species 1986 1986 1986 1986 1987 1987 1987 1987

Barbus graellsii Barbus haasi Chondrostoma toxostoma Noemocheilus barbatulus Rutilus arcasii Oncorhynchus mykiss

4 4 4 4 4 4 4 4 4 4 3 3 3 3 3 3 4 4 4 4 4 4 4 4 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 2 4 1 0 0 0 0 0

Number of days estimates were made 3 2 2 1 2 2 2 2

142

Microhabitat use in the upper Rio Matarraiia

Habitat a v a i l a b i l i t y

AB6, ES87, 11(15 L M 5

IF - - - - - - - * - * - . . - - 1

2

I -2 - 1 0 1 -4 - 3 -

0- 985 - - % S i l t (0.61) % Alaae & Dobrls (-0.76)

Fig. 1. Seasonal changes in microhabitat availability and microhabitat use for B. graellsii, B. haasi, Ch. toxostorna and 0. mykiss. Seasons connected by bars are not significantly different. Open circles are significantly different from the season identified at the right of the bar. Axis loadings >0.40 are presented. Sea- sonal abbreviations are as follows: ES84 - early summer 1984, LS84 - late summer 1984, W84 - winter 1984, 585 - spring 1985, LS85 - late summer 1985, A85 -autumn 1985, W85 - winter 1985, S86 - spring 1986, ES86 - early summer 1986, LS86 - late summer 1986, A86 - autumn 1Y86, S87 - spring 1987, ES87 - early summer 1987, A87 - autumn 1987.

-3 -2 - 1 0 1 2

o------ES87, WB5

0 Alone 6 D.brIs ( -0 .48) % Silt (0.76)

Barbus haasi

LSOS

1 -4 - 3 -2 -1 0 1 2 *x- LsW

4j- ES87

% Algae Oebris (-0.55) 0 S i l t (0 .64)

Ghondrostoma tOX0StOma

- 4 -3 - 2 - 1 0 1 2

LSW, L584, €884

%Algae and debris ( -0 .67 ) % S i l t (0.641

Oncorhynchus mykiss

LS85 S85 €888 w 4 WE5

I I \ I I a

I 1- I I w- - 4 -3 - 2 - 1 0 1 2

Dist. from sub. (0 .80)

% Alpae 6 Debris (-0.45)

96 Rubble (0.44)

Ave. Wl. (0 .45)

Focal pt . vO1. (0 .41)

% S i l t (0.43)

143

6 E 0 %

f Ta

ble 2

. Com

pone

nt s

core

cat

egor

ies in

whi

ch n

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micr

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for

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r Mat

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hes.

Data

pre

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ed a

re fr

om c

ateg

ories

that

wer

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her s

ignific

antly

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r- or

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alysis

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s 20

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(in p

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om m

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ats

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El

Scor

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Seas

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Si

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s

Num

ber

exhib

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nonr

ando

m

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Over

(R)

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un

der (

U)-

repr

esen

ted

Sprin

g 19

86

Avail

abilit

y da

ta

20

2a

-1.5

to

3.5

6. g

rael

lsii

24

2 -1

.0 t

o 3.0

3

-3.0

to

1.5

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.0 t

o 1.

5

Early

sum

mer

198

6 Av

ailab

ility

data

31

1

-2.0

to

2.5

2 -2

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3

-2.5

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2.0

6. g

rael

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21

1 -1

.5 t

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1.5

3 -3

.0 t

o 0.5

3

B. h

aasi

15

1 -0

.5

to 2

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3 -1

.5to

0.5

1 2 -1

.0 t

o 0.5

3

-3.5

to

1.0

3 0.

myk

iss

14

1 0.0

to

2.0

2 -1

.5

to 0

.5

3 -1

.5

to 1

.0

Avail

abilit

y da

ta

24

1 -2

.0

to 2

.0

2 -2

.0 t

o 2.

5 3

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to

3.0

B. gr

aells

ii 25

1

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to

2.0

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3 -1

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o 3.0

8. ha

asi

19

1 -2

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o 1.5

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to

0.5

Ch

. tox

osto

ma

28

1 -2

.0

to 2

.5

2 -3

.5 t

o 2.0

3

-1.5

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1.5

Ch. t

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a 29

1

-1.0

to

1.5

Late

sum

mer

198

6

N. b

arba

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s 7

1.5

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.0

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.5

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5 7 10 9 7 5 7 11 8 14

15 6 15

10 8 6 4 4 8 12 4 6 9 10 a

R R R R R R R R R R R R R R R R

&

Aver

age

Yo e

veloc

ity

Dept

h Yo

Yo

YO

%

%

%

algae

/ v1 3

(crn

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(crn

) be

droc

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grav

el sa

nd

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42 (

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(0.4

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(-0.4

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0 11

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91

1

3

11 (0

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44

(0.6

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13

50

0 12

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14

39

4 (0

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34

4

(0.7

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(0.4

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(0.5

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(0.7

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1 6 33

0

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1 33

0

3 28

0

4 0

no s

ignific

ant

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gorie

s

0 46

7

(0.8

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14

25 (

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0)

3 (0

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(0

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(-0

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(0

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(0

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(-0

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(0

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7

17

14

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13

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13

2

0 2

19

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9

0 44

13

6

19

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0 44

5

13

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13

18

8 49

14

8

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(0.6

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16

1 2

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0 0

47 (

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10 (-

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) (-0

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(0

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79

21

22

7 14

11

71

25

23

72

27

15

17

Autu

mn

1986

Av

ailab

ility d

ata

23

1 2 3 B.

grae

llsii

20

1 2 6.

haa

si 13

3

Cb. f

oxos

fom

a 29

1 1 2

Sprin

g 19

87

Avail

abilit

y dat

a 25

1 2 3

5. gr

aells

ii 23

2 3 3

5. ha

asi

12

1 2 3 Cb

. fox

osfo

ma

25

1 3

Early

sum

mer

198

7 Av

ailab

ility d

ata

25

1 2 3 B.

gra

ellsi

i 22

1 1 3

5. ba

asi

15

1 3 Cb

. fox

osfo

ma

29

1 1 2 3

Avail

abilit

y dat

a 30

1 2

6. gr

aells

ii 28

1 1 2

6. ba

asi

61

Cb

. fox

osfo

ma

27

1

Autu

mn

1987

-2.5

to

2.0

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to

3.5

-2.5

to

2.5

-2.5

to

0.5

-1

.0

to 4

.5 -0

.5

to 1

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-2.5

to

1.5

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to

4.5

-2.5

to

2.0

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to

3.0

-2.0

to

2.0

-2

.0

to 3

.0

-3.0

to

1.0

-1

.5

to 2

.5

-1.0

to

1.5

-1

.0

to 2

.0

0.0

to 2

.5

-1.0

to

2.5

-1.5

to

2.5

-1.5

to

2.5

-3.0

to

2.0

-2.0

to

3.0

-2.0

to

2.0

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to 3

.5 -1

.5 t

o 1.

5 -1

.0 t

o 2.

0 -1

.5 t

o 2.5

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to

2.0

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to

4.5

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to

3.0

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to

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0 9

0.0 t

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0.5 t

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0 9

-0.5

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15

I .o

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8

1 .o to

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8

0.0

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8 0.

5 to

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5

0.5

to 2

.5

10

0.5

to 2

.0 13

1.5

to 2

.5 10

-1.0

to

-0.5

9

0.0 t

o 0.5

5

1 .o to

2.0

7 0.5

to

1.5

9 -1

.0

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.5

7 0.5

to

1.5

7 0.

0 to

0.5

6 1.

0 to

2.5

10

2.5 t

o 4.

5 6

-1.0

to

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4

0.5

to 1

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10

2.5

to 3

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6 1.

0 to

1.5

7

0.5

to 3

.0

6 1.

0 to

3.5

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10 (0

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33

(-0.

52)

5 (0

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(0

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4

56

35

3 54

10

23

0

18

60

73

(-0.9

2)

43 (-0

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42

60

16

25

4 28

3 (-0

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42

(0.7

0)

(0.4

5)

(-0.5

4)

(--0.

46)

12

51

6 4 48

13

19

0

61

18 2

45

0 1

9 (0

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5

(0.5

9)

(0.5

2)

2 6 1 6

4 2 2

20 (-

0.73

) 15

(-0.

43)

(-0.

61)

(0.5

4)

30

2 3 9 35

32

19

11

3 11

22

2 (0

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(0.4

9)

(-0.4

8)

0 9 0 0 0 0 0 0

3 (0

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35

(-0

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21

(-0.

56)

13 (-

0.41

) 14

(0.8

6)

(-0.5

5)

(0.6

2)

(0.6

6)

(-0.5

6)

(0.4

0)

11

28

22

0 19

0

4 0

16

31

14

10

16

33

12

0 15

0

7 10

15

37

0

25

12 (0

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(0.4

2)

26

12

28

27

33

39

7 (-0

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39

(0.5

6)

3 (0

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39

(-0.

65)

8 (-0

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15

(-0.

52)

21 (0

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13

(0.7

6)

(0.7

2)

(0.4

3)

(0.5

9)

(-0.7

3)

(0.4

2)

(0.6

7)

5 62

20

29

11

3

24

8 5

2 45

6

33

4 17

25

0

21

0 9

55

0 5

70

27

2 59

73

53

1 51

5

8 19

17

15

4

5 31

21

13

19

ti’

18 (-

0.82

) 2

43 (

-0.6

2)

28

12

5 (0

.91)

7

(0.9

2)

(-0.6

7)

(0.7

4)

(0.4

3)

1 z

(0.4

6)

5 21

5

12

21

22

28

23

3 13

22

22

5 0

29

47

F 3

21

27

14

3 3 ii

* O

ini0

.5. a

No

selec

tion

occu

rred

on c

ompo

nent

1.

Data

are

pre

sent

ed o

nly

for v

ariab

les w

ith lo

adin

gs 2

0.40

. No

fish

obs

erva

tions

; dat

a fro

m h

abita

t ava

ilabi

lity

quad

rats

. u

* V

I cp


differ significantly during these periods, indepen- dent of changes in mirohabitat availability. We used seasonal intraspecific CADS of microhabitat use for these comparisons.

5 -

0

Results Annual variation in numerical abundance

Over the entire study period, the mean abundance classes for all species ranged from 1.8 to 3.0 (Table 1, 1986-1987 data). The mean abundance was consistently higher in 1984-1985 (2.4-3.0) than during 1986-1987 (1.8-2.8). The decreases noted in the latter two years were attributable to declines in abundance of 0. mykiss and Barbus haasi.

We observed the following changes in intraspecific abundance during 1984-1987. Both B. graellsii and Ch. toxostoma were extremely abundant, and their numbers never dropped below 4 on the categ- orical abundance scale (1986-1987 data in Table 1). The abundance of B. haasi declined during 19861987 (Table 1). Adult 0. mykiss became common in winter 1984 due to their introduction into the site. Their abundance subsequently declined, however (Table 1). Although we recorded young-of-the-year 0. mykiss during early summer 1986, they were not observed during subsequent sampling periods. These young-of-the-years were the result of successful reproduction (in spring 1986) by adult trout stocked in winter 1984.

I I I I

Annual and seasonal changes in microhabitat availability

The CAD extracted a single axis with a variance ratio of 0.88 (Fig. 1). For purposes of clarity, we interpreted this axis rather than the 70+ significant pair-wise differences produced by univariate analyses. This analysis indicated that the study site contained more silt and less algae/debris during spring 1985, and early and late summer 1986, than in the majority of the remaining seasons. The converse was true for late summer 1985 (i.e., more algae/debris and less silt than most seasons, Fig. l). Due to its higher elevation and closer proximity to springs and other sources of subsurface flow, the upper site was less affected by the drought of 1984-1986 than the lower site (Fig. 1).

5 -

0

lntraspecific microhabitat use

We will present only a general description of the results due to the extensive tabular presentation of the data (Table 2). The PCA always extracted a majority of the variance in the data set (X=74%, range 6679%)). The average percentage variation explained by individual components varied by season (PC l X and range=39, 3346%, PC 2 X and

I

range=20, 17-24%, PC 3 x and range=15, 13- 18%). These components described either depth ~

velocity ~ substratum gradients (PC 1 for all sea-

5 -

0

Early Summer 1986

I I

15 n = 31

lo \ Habitat

-2 -1 0 1 2 3 - I Silt (-0.90) % Gravel (0.84)

% Algae and debrls (0.81) Current velocity (0.78)

n 21 Barbus graellsii

10

5 -

0 I , I I I

-2 -1 : o ' 1 2 3

l5 1 Barbus haasi n = 15

lo 1 -2 -1 0 1 2 3

Chondrostoma toxosloma n = a l5 1 10

5

0

-2 -1 0 1 2 3

Oncorhynchus myklss n=14 10

-2 -1 0 1 2 3

Score on Component 1 Fig. 2. An example of the graphical results produced by the PCA test for nonrandom microhabitat use (results from early summer 1986). Histograms depict frequency distributions of component scores for microhabitat availability (top) and fish use data. Variables with loadings >0.40 are displayed (loadings in parentheses). Hatched bars represent categories that were significantly overrepresented with a partitioned chi-square analysis.

146

Microhabitat use in the upper Rio Matarrafia

in B graellsii, B. haasi, Ch. toxostoma were related to changes in microhabitat availability (Fig. 1). For brevity, these results will not be reported. 0. mykiss occupied shallower microhabitats with higher average and focal point velocities and more rubble during winter 1984, 1985 and early summer 1986 than in spring and late summer 1985 (Fig. 1). This species also occurred in areas with increased algae/ debris and less silt during spring 1985. B. haasi also occupied microhabitats with higher quantities of algae/debris and less silt in spring 1985 and early summer 1986, whereas the opposite was true for late summer 1984 (Fig. 1). Similarly, both B. graellsii (Fig. 1) and Ch. toxostoma (Fig. 1) were found in locations with increased algae/debris and less silt during spring 1985, whereas the opposite was true for the remaining seasons.

sons) or substratum gradients with the occasional inclusion of depth and velocity (PCs 2 and 3, Table 2).

Both B. graellsii and Ch. toxostoma generally occupied deeper microhabitats with low to average velocities, higher amounts of depositional substrata, and lower quantities of erosional substrata (Fig. 2, Table 2). On occasion a different pattern was exhibited by B. graellsii (i.e., autumn 1986, PC 1, Table 2). B. haasi tended to avoid microhabitats with rubble substrata and occupied locations with higher amounts of algae/debris (Table 2). Finally, 0. mykiss occurred in shallower areas with slightly higher velocities, and a heterogeneous substratum. In general, nonrandom microhabitat use by assemblage members was similar throughout the study.

Annual and seasonal changes in intraspecific microhabitat use

Seasonal CADS of microhabitat use extracted substratum-related axes for B. graellsii, B. haasi and Ch. toxostoma (Fig. 1). A majority of annual and seasonal changes in nonrandom microhabitat use

Size-related changes in microhabitat use

B. graellsii, B. haasi and Ch. toxostoma all exhibited size-related variation in microhabitat use during 1984-1987. Smaller B. graellsii tended to occupy shallower microhabitats with slower velo-

Table 3. Size-related differences in microhabitat use. We tested univariate data or CAD scores for size effects using Mann-Whitney and Tukey-Kramer tests. Only variables with loadings 20.40 are presented for the CAD.

~ ~~~

Mann-Whitney Tukey- Mann-Whitney Tukey- tests on Kramer CAD Variance tests on Kramer

Species Season Size groups Variables univariate data tests axes ratios CAD scores tests

8. graellsii Spring 1986 518, 219 Bedrock (0.95) 1 1.53 3.46''' 1 8 4 9 Silt (-0.70) Depth (0.64) Rubble (-0.64) Gravel (-0.82) Sand (-0.54)

Early summer 1986 4 9 , 220 Depth 2.10' 19<20 Autumn 1986 518, 219 Algaddebris 2.14* 1 8 4 9 Spring 1987 4 8 , 219 Focal point velocity 2.17* 18<19

Sand 2.07' 19<18 Early summer 1987 4 8 , 219 Depth 2.20* 1 8 4 9

Sand 2.03* 1 9 4 8 Autumn 1987 518, 219 Distance from substratum 2.35* 1 8 4 9

____

8. haasi Spring 1986 57, 2 8 Focal point velocity (0.95) Average velocity (0.79) Silt (-0.73)

1 1.40 3.02"' 7-3

Ch. toxostoma Spring 1986 59, 210 Depth (0.88) Distance from shelter (0.78) Focal point velocity (0.66) Silt (-0.62) Bedrock (0.59) Algae/debris (0.58) Average velocity (0.57)

Silt (-0.69) Rubble (0.67) Gravel (0.60)

Early summer 1986 59, 210 Distance from shelter (0.80)

9<10 1 1.63 3.99***

1 1.23 4.02"' 9<10

* R 0 . 0 5 ; * * P<O.Ol; * * * k 0 . 0 0 5 .

147


cities and greater amounts of sand (Table 3). These differences may have produced the heterogeneous response in non-random use observed in spring 1987 (Tables 2, 3). Smaller B. haasi were found at lower focal point and average velocities during one season, spring 1986. Smaller Ch. toxostoma occurred closer to refuges and over greater amounts of silt in spring and early summer 1986. Smaller Ch. toxostoma also occupied shallower areas with lower focal point and average velocities in spring 1986.

Intersite differences in microhabitat availability and use

The upper site possessed a more heterogeneous substratum than the lower site during the 4 years of our study (Table 4). The upper reach always contained greater amounts of sand than the lower

site, whereas the converse generally was true for algae/debris (Table 4). In addition, algae/debris in the upper side consisted primarily of debris. whereas in the lower site it was dominated by a filamentous alga (Cfadophora). The remaining substrata varied in an inconsistent manner. When velocity differences were observed (3 seasons), average velocities in the upper site always were greater than those in the lower reach. Although average depth in the upper site was greater than the lower site in spring and late summer 1986, the opposite occurred in autumn 1986 and spring 1987.

Most intersite differences in microhabitat use for B. graellsii and Ch. toxostoma were related to differences in substratum availability (Table 4). Both species occurred closer to the substratum in the site with higher velocities (ix., upper site). This response was more pronounced in Ch. toxostoma.

Table 4. Intersite difference in habitat availability and microhabitat use for 24 6. graellsii and Ch. toxosfoma. Presented are variable loadings (20.40) for CAD axes. For all seasonal intersite comparisons U=upper site, L=lower site.

Spring Early summer Late summer Autumn Spring Early summer Autumn 1986 1986 1986 1986 1987 1987 1987

Microhabitat availability Average velocity Depth Bedrock Rubble Gravel Sand 0.92 Silt

Site with significantly greater CAD score

Algae/debris -0.79

U

0.77 0.64 -0.42 -

0.81 0.53 -0.70 0.89 0.83 0.85 0.71 0.90 0.79

-0.99 -0.69

U U U

0.42 0.65 -0.70

0.63 0.63 0.90 0.69

0.85 -0 87

U U U

B. graellsii Average velocity Focal point velocity Depth Relative depth Bedrock Rubble Gravel Sand Silt Algae/debris

Greater site

0.75 0.72

-0.56

0.77 0.68

0.65 0.56 0.95

0.60

0.44

-0.72 -0.98

U U

0,88 0.54 0.73 0.51

0.80

-0.51 -0.42 -0.54 -0.70 -0.78

0.79

U L

0.68 0.69 -0.69

0.48 0.66 0.46

0.61 0.67 -0.95

L U L

-0.70 0.73 -0.79

Ch. toxostoma Average velocity Focal point velocity Depth Relative depth Rubble Gravel Sand Silt Algae/de bris

Greater site

0.76 0.73

0.69 -0.60

0.71 0.87 0.59

0.59 0.88

-0.63 -0.99

U U

0.95 0.71 0.56

~0.53 -

U

0.60 0.76 0.72

-0.72 0.50

-0.84 0.65 -0.67 0.79 0.60

U L

0.51 0.63

-0.84 0.41

0.77 0.49

-0.92

U

* No Ch. toxosfoma were observed in the lower site during this season.

148

Microhabitat use in the upper Rio Matarraiia

Table 5. Interspecific differences in microhabitat use. We conducted Kruskal-Wallis tests on univariate data or CAD scores for each species and then used Tukey- Kramer tests to identify significant pairwise differences. Only variable loadings 20.40 are presented for the CAD. Species abbreviations are as follows: BG=B. graellsii, BH =B. haasi, CT= Ch. toxostoma, NB=Noemchei/us barbatulus, OM= 0. mykiss.

Season Variables

~

Kruskal-Wallis Kruskal-Wallis

univariate data tests axes ratios axis scores results tests on Tukey-Kramer CAD Variance tests on Tuker-Kramer

Spring 1986

Early summer 1986

Late summer 1986

Autumn 1986

Spring 1987

Early summer 1987

Autumn 1987

Distance from substratum Distance from shelter Silt Algaeldebris Depth Gravel Depth Distance from substratum Sand Distance from substratum (0.93) Distance from refuge Depth Distance from substratum Gravel

Focal point velocity Distance from substratum Gravel Depth Average velocity Distance from substratum (0.90) Distance from shelter (0.72) Depth (0.61) Sand (-0.48) Distance from substratum Depth Average velocity Distance from shelter

20.79"' 15.36* * * 12.70*** 10.78*" 8.15* 19.13*** 16.19**' 12.27' 10.48*

19.50* 16.65'* * 11.74*** 9.22.' 14.25* * 13.87** * 13.70* * * 7.73* 6.68*

8.86* 7.64* 6.36' 6.28'

BG, CT>BH BG. CT>BH BH, CT>BG Bh, CT>BG BG>BH, CT

BH. OM>BG, CT BG. CT<OM C T S H , OM

OM>BG 1 2.835 4.65*** BG, CT>BH, NB

C T S G , BH CT>BG, BH CT>BG, BH

B H A T

BG, B H X T BG, CT>BH BH>BG, CT

BG>BH B H X T

1 1.48 31.49*** BG, CT>BH

BG, CT>BH CT>BH BGrBH BG>BH

* R 0 . 0 5 ; * * RO.01; * * * R0.005.

lnterspecific differences in microhabitat use

As with the lower site, distance from the substratum proved to be the best discriminator of interspecific differences in microhabitat use (Table 5). B. graellsii and Ch. toxostoma did not occupy statistically differentiable microhabitats in four of seven seasons (early summer 1986, late summer 1986, early summer 1987 and autumn 1987). In the remaining seasons, these 2 species differed in their use of at least one microhabitat parameter (Table 5). These differences were not consistent, however (i.e., B. graellsii occupied deeper areas than Ch. toxostoma in spring 1986, whereas the converse was true in autumn 1986). 3. graellsii did occur in microhabitats with faster focal point velocities in spring 1987 and closer to the substratum and refuges during autumn 1986 than Ch. toxostoma. In general, however, these 2 species do not appear to have strongly differentiated microhabitat preferences.

B. haassi typically occurred closer to the substratum and refuges, and in shallower locations with more gravel than the remaining species (Table

5) . Microhabitat use of Noemacheilus barbatulus was not significantly different from that of B. haasi during the one season in which it was present. 0. mykiss occurred in shallower microhabitats with more gravel during early summer 1986 than B. graellsii and Ch. toxostoma. It was found closer to the substratum than Ch. toxostoma and over san- dier microhabitats than B. graellsii (Table 5).

Assemblage members did not occupy statistically distinct microhabitats during seasons when 0. mykiss was both present and absent (Fig. 1). Consequently, the presence of 0. mykiss appeared to have little effect on the use of spatial resources in this assemblage. A similar lack of effect can be postulated for B. haasi, which declined in abundance during the last 6 seasons of the study, with a concomitant lack of microhabitat shifts in the remaining species.

Discussion

Both intraspecific and interspecific patterns of microhabitat use by members of the upper Matar-

149


raiia fish assemblage remained relatively constant during a 4-year period of observations. The species native to the system occupied deeper microhabitats with a heterogeneous substratum. In general, nonrandom use of substrata was attributable to co- variation of these parameters with depth and velocity, a phenomenon also observed in the lower Matarraiia (Grossman & de Sostoa 1994). Sea- sonal and annual differences in microhabitat use for all species generally were correlated with changes in microhabitat availability, although B. graellsii and 0. mykiss exhibited annual changes in their use of velocity and erosional substrata. In addition, B. haasi, however, was not as strongly affected by depth in the latter two years of the study as it was during 1984-1985 (Table 2, Grossman et al. 1987b). These variations generally were not consistent among years, and their biologi- cal significance is unknown.

Size-related disparities in microhabitat use for B. haasi and Ch. toxostoma were more pronounced during 1984-1985 than in the latter 2 years of the study (compare Table 3 with Table 4 of Grossman et al. 1987b). This may have been due to the smaller sample sizes obtained during 1986-1987 (compare Table 2 with Table 3 of Grossman et al. 1987b). Conversely, we observed size-related differences in microhabitat use for B. graellsii more fre- quently in the last 2 years of the study. In addition, these differences involved dissimilar variables. In 1984-1985, substratum variables were most im- portant to size-related disparities in microhabitat use by B. graellsii, whereas in 19861987 depth played a stronger role in size-related differences. Size-related differences in microhabitat use by B. graellsii and Ch. toxostoma were similar in both upper and lower sites.

Most size-related differences in microhabitat use of assemblage members can be explained by the enhanced physical capabilities of larger specimens, which enable them to occupy: faster velocities, deeper locations farther from the substratum and shelter and areas with greater quantities of larger erosional substrata. Similar patterns (i.e., larger specimens occurring in more energetically costly microhabitats) have been reported for a variety of stream fishes in both Europe and North America (Grossman & Freedman 1987; Heggenes & Traaen 1988; Simonson & Swenson 1990; Hill & Grossman 1993). Several investigators have shown that size-related shifts in depth distribution are produced by the increased predation pressure ex- perience by smaller fishes in deep water (Schlosser 1987; Power et al. 1989; Harvey & Stewart 1991). In the upper Matarraiia, however, the only common predators are water snakes (Natrix natrix and N. maura) that hunt from the banks of the stream.

Hence, it is unlikely that the observed pattern of smaller specimens occupying shallower areas is linked to a reduction in predation pressure.

Intersite differences in microhabitat use were similar throughout the 4 years of study. Most substratum-related changes were due to intersite differences in substratum availability. Both B. graellsii and Ch. toxostoma occurred closer to the substratum in the site with faster average velocities (i.e., upper site). The response of Ch. toxostoma to this parameter was stronger than that of B. graellsii. This behavior probably reduces the energetic expenditure associated with maintaining posi- tion in habitats with higher mean velocities (Fa- cey & Grossmann 1990, 1992) and has also been observed in several species of salmonids (Heggen- es & Saltveit 1990; Rincon & Lobon-Cervia 1993).

Patterns of interspecific microhabitat use were similar throughout our study, with B. graellsii and Ch. toxostoma occupying mid-water column microhabitats and B. haasi occurring on or near the substratum. In general, B. graellsii and Ch. toxostoma did not occupy markedly distinct microhabitats. Although some authors have reported strong microhabitat segregation in stream fish as- semblages (Gorman 1988), other investigators have demonstrated substantial overlap in habitat use by stream fish (Grossman & Freeman 1987; McNeely 1987; Brown & Moyle 1991). Our results from the upper Matarraiia demonstrate that 2 of the 3 common speices exhibited strong similarities in their use of space over a 4-year time span. Hence, microhabitat segregation does not appear to be required for coexistence of B. graellsii and Ch. toxostoma in the Rio Matarraiia.

Neither the introduction of 0. mykiss nor the general decrease in abundance of B. haasi produced microhabitat shifts in the native species. The decline in B. haasi mirrored decreases of G. gobio and Ch. toxostoma in the lower site and may have been due to prolonged low water conditions present during of 1984-1985 and portions of 1986 (Grossman & de Sostoa 1994). Such conditions have been shown to produce declines in the abundance of stream fishes (Grossman et al. 1982). 0. mykiss was not present in the study site after early summer 1986, and its disappearance may have been related to increased fishing mortality (per- sonal observation). We are unable to explain the disappearance and presumed high mortality of young-of-the-year 0. mykiss during early summer 1986, however. This may be related to some environmental characteristic, because naturally re- producing populations of 0. mykiss are uncom- mon in Spain (de Sostoa unpublished work). Microhabitat use patterns of adult and young-of- the-year 0. mykiss were distinct, and these differ-

150

Microhabitat use in the upper Rio Matarrafia

5. Las diferencias entre localidades en el us0 de microhabitats por B. graellsii y Ch. toxostoma mostro que las mayores diferencias en el us0 del sustrato se debieron a disparidades en la dis- ponibilidad de sustratos. Ambas especies ocurrieron mas cerca del sustrato en la localidad con mayor velocidad de agua (localidad aka), aunque esta respuesta fuC mas pronunciada en Ch. toxostoma. Sin embargo, no ocuparon microhibitats estadisti- camente diferenciables aunque ambas aparecieron siempre mas lejos del sustrato y de refugios que B. haasi. 0. mykiss ocupo microhabitats mas someros y con mas grava que B. graellsii y Ch. toxostoma. 6. La falta de cdmbios observados en el us0 de microhabitats por las especies nativas durante el periodo de estudio indica que las interacciones con B. haasii o con 0. mykiss no juegan un papel relevante en el us0 de microhabitats por parte del resto de 10s miembros del ensamblaje.

ences resulted in a reduced ability to discriminate 0. mykiss from the remaining species when only young-of-the-year were present (i.e., early summer 1986).

In conclusion, despite the introduction of a highly aggressive, exotic species (0. mykiss) and the decline of a native species (B. haasz], the remaining member of the Rio Matarraiia did not display shifts in microhabitat use. The effects of B. graellsii and Ch. toxostoma on 0. mykiss and B. haasi remain unknown. Nonetheless, given the high microhabitat overlap and plasticity observed in this assemblage and the lack of observed interspecific aggression and niche shifts, it is unlikely that interspecific competition plays a strong role in determining the pattern of microhabitat use by fishes in the upper Rio Matarraiia. In contrast, the dominant species appear to have extremely flexible microhabitat requirements as demonstrated by their long-term population growth and persistence in the disparate habitats of the upper and lower Matarraiia (de Sostoa et al., unpublished work).

Resumen 1. Desde 1984 a 1987, evaluamos la abundancia y el us0 de microhabitats de Barbus graellsii, B. haasi, Chondrustoma to- xastoma, Noemacheitus barhatulus, Oncorhyncus mykiss, y Ruti- lus arcassi en la zona aka del Rio Matarraiia. Para todas las especies, la abundancia media oscilo entre 1.8 y 3.0, donde 1 = 1-5, 2 = 6 1 0 , 3= 11-20 y 4220 individuos, respectivamente. La abundancia media fue mayor en 19841985 (2.43.0) que en 1986-1987 (1.8-2.8). Esta reduccion se debio a1 descenso de 0. mykiss que habia sido introducida en el invierno de 1984. Sin embargo, B. graellsii y Ch. toxostoma fueron abundantes a lo largo de 10s cuatro aiios de estudio y solo observamos de forma irregular a N. barbatulus y R. arcasii. 2. El analisis de 10s datos de microhabitat indico que la zona de estudio tuvo mayores cantidades de limo muy fina y menos de algasidebris durante la primavera de 1985 y a1 principio y final de 1986, que en el resto de las estaciones y aiios estudia- dos, mientras que lo contrario ocurrib a1 final del verano de 1985. 3. Un analisis de componentes principales mostro que B. graellsii y Ch. toxostoma ocuparon microhabitats mas profundos con velocidades de agua bajas o moderadas, mayores cantidades de sustrato de deposit0 y menores de sustrato erosivo. B. haasi parece rechazar microhabitats con sustrato de piedras de tamaiio medio y aparecio en aquellos con altas cantidades de algasi debris. 0. mykiss ocup6 aguas someras con velocidades de agua algo altas y sustrato heterogeneo. 4. Con la excepcion de B. haasi, 10s microhabitats utilizados por todas las especies fueron similares a lo largo del periodo de estudio. Sin embargo, B. haasi no estuvo tan influenciado por la profundidad en 10s dos ultimos aiios como lo estuvo en 1 9 8 4 1985. El analisis de las variaciones estacionales y anuales del us0 de microhabitats entre las especies, mostro que la mayor parte de 10s cambios se debieron a variaciones en la disponibili- dad de microhabitats. Sin embargo, todas las especies mostra- ron cambios minimos en el us0 de estos microhabitats. El analisis de cambios relacionados con el tamaiio seiialo que 10s individuos menores de B graellsii y Ch. toxostoma ocuparon microhabitats mas someros con velocidades menores que 10s individuos mayores.

Acknowledgements The acknowledgements are identical to those presented in Grossman & de Sostoa (1994).

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Documents

Microhabitat use by fish in the upper Rio Matarraña, Spain, 1984–1987