Size-related and diel variations in microhabitat use of
three endangered small fishes in a Mediterranean
coastal stream
M. C L A V E R O *†‡, F . B L A N C O -G A R R I D O †, L . Z A M O R A *
J. PRE NDA †
AND
*Institut d’Ecologia Aqua`tica, Universitat de Girona, Facultat de Ciències, Campus
Montilivi, 17071 Girona, Spain and †Departamento de Biologı´a Ambiental y Salud
Pública, Universidad de Huelva. Campus Universitario de El Carmen, Avda.
Andalucı´a s/n, 21071 Huelva, Spain
This study analysed the microhabitat use of three endangered fish species, Andalusian toothcarp Aphanius baeticus, Iberian loach Cobitis paludica and sand smelt Atherina boyeri, in a
coastal stream stretch. Plastic minnow traps were set both during daytime and at night on the
bottom and at the surface. Depth and presence of effective refuge were recorded for each trap.
To assess size-related changes in microhabitat use individuals of each species were classified in
three size classes. The three species preferentially used bottom positions in the water column,
though this behaviour was more evident in the case of Iberian loach. While large Iberian loach
remained active at night Andalusian toothcarp and sand smelt were strongly diurnal, especially
larger individuals. The three species showed a clear ontogenetic change in microhabitat preferences towards deeper waters. Small Andalusian toothcarp and medium-sized Iberian loach
used deeper microhabitat in the presence of refuge. Large Andalusian toothcarp consistently
preferred exposed microhabitat at any time. Andalusian toothcarp using refuge were smaller at
any time, while Iberian loach followed this pattern only at night. The differential vulnerability
of these species to different predators (aerial and aquatic; diurnal and nocturnal) could explain
the observed patterns in microhabitat use. Fish tended to co-occur in microhabitats either due
to habitat characteristics independently of species or due to species independently of habitat.
Andalusian toothcarp segregated spatio-temporally from sand smelt and Iberian loach, but
these species occurred independently of each other. According to these co-occurrence patterns,
Andalusian toothcarp would be more sensitive than Iberian loach or sand smelt to interspecific
interactions.
Key words: activity; depth; habitat use; interspecific interactions; stream fishes; vegetation.
INTRODUCTION
Fish habitat requirements are determined by factors operating at multiple scales,
running from hundreds or thousands of kilometres (e.g. drainage characteristics)
to centimetres (e.g. presence of macrophytes) (Poizat & Pont, 1996). At the
microhabitat scale of observation (Dungan et al., 2002), fishes have been
shown to select habitat mainly as a function of food availability and predation
‡Author to whom correspondence should be addressed. Tel.: þ34 972 418467; fax: þ34 972 418150;
email: miguel.clavero@udg.es
risk (McIvor & Odum, 1988). Both factors vary during a fish’s ontogeny, causing
changes in habitat preferences (Rosenberger & Angermeier, 2003; King, 2004).
On the other hand, both food availability (Copp et al., 2005) and predation risk
(Schlosser, 1988) can differ from daytime to night. In fact, the equilibrium of risks
due to differential predation by piscivorous fishes and wading and diving terrestrial predators, which is often cited as the cause of the larger fish-deeper habitat
pattern (Power, 1984; Harvey & Stewart, 1991), is likely to differ at night. It is
therefore important to consider the possible ontogenetic and diel variations when
analysing microhabitat use patterns by fishes (Copp & Jurajda, 1999).
Few studies have analysed fish habitat use in Mediterranean streams and they
have focused mainly on widespread cyprinid species (Grossman et al., 1987a, b;
Rincon et al., 1992; Santos et al., 2004). This study analyses the microhabitat
preferences of three small stream fish species: the Andalusian toothcarp
Aphanius baeticus Doadrio, Carmona & Fernandez-Delgado, henceforth toothcarp, Iberian loach Cobitis paludica de Buen, henceforth loach, and sand smelt
Atherina boyeri Risso. There is hardly any available information on the habitat
requirements of these species at any scale of observation, and none on microhabitat use.
Knowledge of fish habitat preferences is one of the main tools for efficient fish
conservation and fisheries management. In the case of these three species the
scarcity of knowledge is worrying, since they are endangered and should involve
conservation actions (Doadrio, 2001). Loach and sand smelt are considered
‘Vulnerable’ (VU) in Spain following IUNC criteria (Doadrio, 2001).
Toothcarp should be catalogued as ‘Critically Endangered’ (CR), since there
are only eight extant populations, some of them suffering strong declines
(Doadrio et al., 2002; Clavero et al., 2005a). The aim of this study was to analyse
the microhabitat use of toothcarp, loach and sand smelt occupying sympatrically
a coastal Mediterranean-regime stream. Passive capture methods (plastic minnow
traps) were employed to assess size-related and diel variations in the microhabitat
preferences of the three species, as well as the patterns of coexistence between
species and size classes.
MATERIALS AND METHODS
S T U D Y A RE A
This study was conducted in the La Vega River (southern Spain), the last water course
of the Iberian Atlantic slope, which flows to the sea through a common estuary with the
adjacent La Jara River (Fig. 1). La Vega River is only 13 km long and has a drainage
area of c. 20 km2, is free of important effluents and does not have regulation infrastructures, thus featuring a natural flow cycle (Clavero et al., 2005b). Due to its small size, this
river suffers extreme flow changes following a typical Mediterranean cycle (Gasith &
Resh, 1999), being reduced to a few isolated pools during the summer. Fish microhabitat
was analysed in a 600 m stretch located just upstream of the tidal section (Fig. 1). Water
flow ceases each year around the beginning of July. After that moment fresh water is
retained only in five pools, some of which are occasionally filled with sea water (Clavero
et al., 2005a). The studied stretch covers all or most of the stream section occupied
sympatrically by toothcarp, loach and sand smelt. While the tidal waters mark the lower
limit of loach distribution, toothcarp was not detected in the upper pool of the study
stretch until the last two surveys.
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
Study site
Tarifa
FIG. 1. Location of the study area.
The presence of both estuarine and freshwater species favours the presence of a rich
ichthyofauna, with at least 11 species, among which there are no introduced species (Clavero
et al., 2005b). Among these species the eel Anguilla anguilla (L.) is the most abundant
piscivorous fish. Other abundant fish predators include viperine snakes Natrix maura, egrets
Bubulcus ibis and Egretta garzetta and kingfishers Alcedo athis. The otter Lutra lutra also
occurs but none of the three studied species is important otter prey (Clavero et al., 2004).
FISH SAMPLING
Eleven surveys were performed between October 2002 and August 2004. Fish microhabitat preferences were studied using cylindrical plastic minnow traps (240 mm long, 95 mm
wide and 21 mm at the mouth), henceforth traps (Hubert, 1996). Traps were fixed to the
stream bottom with a metal stick, through small holes (4 mm). In the last six surveys traps
were set in pairs, with one trap touching the substratum and the other at the water surface.
The depth (cm) of each trap and the presence of surrounding refuge (submerged or emergent
macrophytes, or submerged riparian vegetation) was noted (Prenda et al., 1997). Traps were
set both during daytime and at night. Night traps were set from sunset to early morning
(around sunrise). On some occasions a large amount of captures caused night traps to be set
some hours in the morning. Considering all captured fishes in these traps as ‘night captures’
is a conservative assumption, however, since possible morning captures would tend to
‘homogenize’ daytime and night results. Each captured fish was identified, measured for
total length (LT, mm) and released.
DATA ANALYSIS
Captures were expressed as catch per unit of effort (CPUE), defined as the number of
individuals captured per trap per hour. To assess possible size-related changes in microhabitat use, fishes were classified into three size classes (I, II and III). Intervals used in
this classifications were different for toothcarp (<22, 23–28 and >28 mm) and for loach
and sandsmelt (<30, 30–45 and >45 mm), since the last two species reach larger sizes.
The following variables were calculated for each trap: the CPUE of each species and size
class, the CPUE of each species (all sizes), the CPUE of each size class (all species) and the
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
total CPUE (all fishes). Depth measurements were converted to 5 semi-quantitative categories for the analyses (<20, 21–30, 31–40, 41–50 and >50 cm). This enabled the analysis
of the role of depth in the variation of CPUE and fish size without assuming linear
relationships, as would have been the case if depth had been used as a continuous variable.
Patterns in microhabitat use were analysed using generalized linear models (GLMs) for
CPUE (Crawley, 2002) and ANOVA for fish size (Copp & Jurajda, 1999). Since CPUE is
a variable derived from count data, Poisson distribution as error and log link function
were used. Significance of the different explanatory variables was checked through
comparisons of the change in deviance and d.f. with a w2 distribution (Crawley, 2002).
In order to use similar terms for ANOVA and GLM results, henceforth the term
‘variation’ is used instead of ‘deviance’. To allow comparable interpretations of the
effects of the different independent variables among species and sizes, every independent
variable and all the second order interactions were included simultaneously in each
model. First, the influence of trap position (bottom-surface) and depth in the CPUE
and size of the different species was analysed. All the data from surveys in which surface
traps had not been set were excluded from this analysis. A second analysis assessed the
role of depth and presence of refuge in the CPUE of the different size classes of the three
species and in their size structure across microhabitat, both at daytime and at night. This
second analysis included only data from bottom traps. By including time (day-night) the
possible diel variations in the activity of fishes could be assessed, assuming that captures
in passive traps would increase with increasing fish activity.
The analysis of microhabitat preferences can show that certain species and size classes
are using similar microhabitats. This does not imply co-occurrence, however, since
similar habitats could be used at different moments. To assess possible patterns of cooccurrence among the studied species and size classes a principal components analysis
(PCA) was applied to a matrix of traps x CPUEs of the different species and size classes,
thus treated as nine different ‘species’. Surface traps and traps in which no individual of
any of the three species had been captured were excluded from this analysis. The
interpretation of principal components was made through Pearson correlation and oneway ANOVA analyses. Prior to PCA and subsequent correlation analyses CPUE data
were logarithmically transformed [log10 (x þ 1)]. Only those principal components (PCs)
with eigenvalues >1 were interpreted (Kaiser criterion).
RESULTS
SUMMARY OF CAPTURES
During the study period 857 bottom traps and 395 surface traps were set, for a
total sampling effort of 11 989 traps h—1. Overall 3699 toothcarps (total CPUE 0•31
individuals trap—1 h—1), 1262 loaches (0•10 individuals trap—1 h—1) and 614 sand
smelts (0•05 individuals trap—1 h—1) were captured. These three species constituted
98•7% of total captures. Other species occasionally captured in traps were Iberian
chub Leucisus pyrenaicus Gunther eel, grey mullets Liza spp. and Mugil cephalus L.,
and common goby Pomatoschistus microps Krøyer. Captured toothcarps were on
average smaller (mean ± S.E. 24•5 mm ± 0•1, range 10–56 mm) than sand smelts
(mean ± S.E. 33•3 mm ± 0•3, range 12–70 mm), which were smaller than loaches
(mean ± S.E. 38•6 mm ± 0•3, range 14–95 mm) (ANOVA, P < 0•001).
POSITION IN THE WATER COLUMN
The three studied species were captured more often in bottom traps than in
surface ones (Fig. 2). This difference was especially strong in the case of loach, since
the GLM showed that >20% of the variation in the CPUE of the species could be
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
Log10 CPUE
(individuals trap–1 h–1)
0·25
Toothcarp
Loach
Sand smelt
0·2
0·15
0·1
0·05
0
LT (mm)
60
n = 152
n = 28
n = 602
n = 38
n = 1993
n = 495
45
30
15
≤20 25
35
45 >50
≤20
25
35
45 >50
≤20
25
35
45 >50
Depth (cm)
FIG. 2. Differences in CPUE and fish size (mean ± S.E.) between bottom (*) and surface ( .) traps at
different depths. Numbers of captured fish are also given.
explained in terms of the position of traps. In contrast, this value was <10% for
toothcarp and sand smelt. The CPUE of loach and sand smelt in surface traps did
not show any clear pattern in relation to depth, but toothcarp were more frequently
captured at the surface when traps were set in shallow waters (Fig. 2).
Sand smelt and toothcarp occupying surface positions were significantly
smaller than individuals trapped at the bottom (ANOVA, P < 0•001 in both
cases), but there was no such difference in the size of captured loach. The smaller
size of toothcarp and sand smelt captured at the surface was a pattern maintained through all depth classes (Fig. 2). Toothcarp and loach occupying surface
positions were larger at night (24•5 and 44•8 mm, respectively) than during
daytime (20•0 and 28•5 mm) (toothcarp F1,494, P < 0•001; loach F1,36,
P < 0•01). Sand smelt did not show such a difference (F1,26, P ¼ 0•8). The
relatively large number of toothcarp captured in surface position (495
individuals) allowed a confident comparison of the relation between fish size
and depth among bottom and surface captures. While the size of toothcarps
using microhabitats near the bottom showed a clear increase with increasing
depth, this pattern almost disappeared in surface captures, which did not present
important size differences among depth classes (Fig. 2).
A C TI V I TY , D EP T H A N D R E F U G E
Toothcarp and sand smelt were captured more frequently in daytime traps
than in those set at night, suggesting a reduced nocturnal activity (Table I). In
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
TABLE I. Results of the GLM on the influence of time (night or day), presence of refuge
(Ref) and depth in the CPUE of the different species and size classes
Factor
d.f.
ToI
ToII
ToIII
Time
1 7 •1 9 • 2
Ref
1 0 •3 0 • 1
Depth
4 13•1
6• 5
Time x Ref
1 0 •2 0 • 0
Time x depth
4 1 •1 0 • 1
Depth x Ref
4 2 •4 3 • 8
Error
835
Total % deviance
24•2 19•9
Dispersion parameter
1 •1 0 • 9
11•0
5 •8
4 •8
0 •1
0 •4
0 •7
22•9
0 •7
LoI
LoII
LoIII
2 •1
0 •3
2 •6
0 •5
1 •2
3 •4
13•8 10•1
0 • 4 0 •2
2• 8
0• 7
7• 0
1• 5
0• 9
0• 8
SaI
SaII
SaIII
1• 4
0• 0
7• 6
0• 3
2• 0
0• 5
6•2 11•1
0 • 0 3 •2
9 • 5 4 •3
0 • 6 0 •4
0 • 2 0 •3
0 • 9 0 •8
11•3
0•2
3•8
0•0
0•2
1•3
11•9
0• 3
17•4 20•1
0 • 2 0 •4
16•8
0•1
To, toothcarp; Lo, loach; Sa, sand smelt. Size classes- I, II and III. Values are the percentage of the
total deviance explained by each factor. Significant results (P < 0•05) appear in bold.
both species these differences in activity between day and night increased from
size I (explaining 6–7% of the total CPUE variation) to size III fish (>11% of
the variation). Size III loaches did not show any significant activity reduction at
night, while the two smaller size classes were slightly more active during daytime.
All toothcarp size classes showed significant preferences for certain depths,
although the strength of this preference decreased from small to large fish
(Table I). During the day size I toothcarps were almost absent at depths
>40 cm, and strongly preferred the shallowest microhabitat. Larger size classes
used relatively deeper microhabitats (Fig. 3). Size III toothcarps clearly preferred
exposed microhabitats, while the presence of refuge allowed smaller size classes
to occupy relatively deeper waters, as shown by the interaction between depth
and refuge (Table I). When using refuge microhabitat at night the three size
classes of toothcarp were more or less equally distributed among depths (Fig. 3).
Loach also showed a change in depth preference towards deeper microhabitats
with increasing fish size. Depth explained a significant amount of the variation in
CPUE only in the smallest and largest loach size classes (Table I), size II loaches
showing intermediate depth preferences (Fig. 3). Loach size classes, however, did
not show absolute avoidance of any depth class as those observed in small
toothcarp. Size II loach occupied deeper positions at any time when using refuge
microhabitats (Fig. 3), though the interaction between depth and refuge was not
significant in the GLM due to a strong underdispersion of the data (Table I).
Data sets on the CPUE of the different size classes of sand smelt were also
severely underdispersed, increasing the probability of type II error (Table I).
Captures of this species were also very low at night, and reliable patterns could
be extracted only from daytime traps (Fig. 3). As with the other species, sand
smelt changed depth preferences from shallow to deeper microhabitats with
increasing fish size. As observed for toothcarp, however, the depth preferences
were stronger in small individuals than in larger ones (Table I). Size II sand
smelts significantly avoided refuge microhabitats.
There were clear direct relationships between fish size and depth in the three
species, but there were also some changes in this pattern related to time and
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
Toothcarp
Day
0·2
Size I
Size II
Size III
Size I
Loach
Size II
Size III
Size I
Sand smelt
Size II
Size III
≤20 25 35 45 >50
≤20 25 35 45 >50
≤20 25 35 45 >50
0·1
Night
0
0·2
0·1
0
Day
0·05
0
0·1
Night
Log10 CPUE (individuals trap–1 h–1)
0·1
0·05
0
Day
0·1
0·05
Night
0
0·1
0·05
0
Depth (cm)
FIG. 3. CPUE (mean ± S.E.) of the different size classes of the three studied species in exposed microhabitats (*) and refuge ones (.) at different depths and times of the day.
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
presence of refuge (Fig. 4). Toothcarp using refuge microhabitat were significantly smaller than those in exposed microhabitat at any time. While during the
day toothcarp in refuge microhabitats were larger in deeper waters this relation
disappeared at night. During the day there were no differences in the size of
loach using refuge or exposed areas, but at night they were larger in the latter. As
with toothcarp, loach did not display a clear size structure in relation to depth
when using refuge microhabitats at night. Loach were also larger in exposed
microhabitat at night than during the day, a pattern that could be observed at
different depths (Fig. 4).
Day
55
Night
n = 1038
n = 1114
n = 605
n = 443
n = 207
n = 238
n = 281
n = 490
n = 243
n = 132
n = 62
n = 101
Toothcarp
45
35
25
15
55
Loach
LT (mm)
45
35
25
15
55
Sand smelt
45
35
*
*
25
15
≤20
25
35
45
>50
≤20
25
35
45
>50
Depth (cm)
FIG. 4. Mean ± S.E. total length in exposed microhabitats (*) and refuge ones ( .) at different depths and
time of the day. Numbers of captured fish are also given. *, less than five valid cases.
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
PATTERNS OF CO-OCCURRENCE
(b)
1·5 (a)
PC4 (12·6%)
III
1
0·5
0
1·5 (c)
1
0·5
0
PC2 (17·8%)
III
II
III
II
I
PC1 (22·7%)
II
I
I
PC2 (17·8%)
Log10 CPUE
(individuals trap–1 h–1)
Log10 CPUE
(individuals trap–1 h–1)
Log10 CPUE
(individuals trap–1 h–1)
PCA was applied to a matrix of 481 rows (traps) x nine columns (species and
size classes) and produced four principal components (PCs) with eigenvalues >1.
PC1 ordered traps as an inverse function of the number of captures [Fig. 5(a)],
was positively correlated with trap depth (r ¼ 0•21; P < 0•001) and its scores
were higher in night traps (ANOVA, P < 0•001). CPUEs of all species/size
classes were negatively correlated with this component, except that of size III
loaches (r ¼ 0•23, P < 0•001), which was the species and size class that had the
maximum nocturnal activity and used the deepest microhabitats among the
different species and size classes. PC4 constituted a gradient running from
traps dominated by size I catches to traps dominated by size III catches
[Fig. 5(b), (d)]. It was positively correlated with depth (r ¼ 0•21; P < 0•001)
and was therefore related to the size-related change towards deeper microhabitat
recorded in the three species (Fig. 3).
PC2 and PC3 scores, however, were not related to habitat use, but with the
specific identity of fishes, independently of fish size. In fact, these two gradients
in trap catches represented trends towards a spatio-temporal segregation
between toothcarp and sand smelt (PC2) [Fig. 5(b), (c)] and between toothcarp
and loach (PC3), while no clear association or avoidance was observed between
1·5 (d)
1
0·5
0
PC4 (12·6%)
FIG. 5. Results of the PCA applied to a matrix of CPUEs of the nine different species and size classes in
481 plastic minnow traps. (a) Relationship between PC1 (eigenvalue ¼ 2•04) and total CPUE
(including all individuals of the three species) (r ¼ —0•91, P < 0•001). (b) Projection of the loadings
of the different species (*, tooth carp, x, loach and ., sand smelt) and size classes (I, II and III) on
the spaced formed by PC2 (eigenvalue ¼ 1•60) and PC4 (eigenvalue ¼ 1•13). (c) Relationship
between the PC2 scores of each trap and the CPUE of toothcarp (*) (r ¼ —0•48, P < 0•001),
loach ( ) (r ¼ —0•09, P ¼ 0•03) and sand smelt (.) (r ¼ 0•80, P < 0•001) independently of size
classes. (d) Relationship between the PC4 scores of each trap and the CPUE of size I (*) (r ¼
—0•66, P < 0•001), size II (x) (r ¼ 0•05, P ¼ 0•22) and size III fish (. ) (r ¼ 0•40, P < 0•001),
independently of fish species.
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
loach and sand smelt. All toothcarp size classes were negatively correlated with
PC2 (P < 0•001 in all cases), while all sand smelt size classes were positively
correlated with it (P < 0•001 in all cases). While CPUE of loach was not related
to PC2, it had a strong correlation with PC3 (r ¼ 0•81, P < 0•001), which was at
the same time negatively correlated with all toothcarp size classes (P < 0•001).
DISCUSSION
POSITION IN THE WATER COLUMN
A strong preference for bottom positions in relation to surface positions could
be observed in the three species under study. This pattern was obvious in the case
of loach that, as other Cobitis species, is a bottom-dwelling fish lacking a
swimbladder (Perdices & Doadrio, 1997), but to date there are no available
data on this issue concerning toothcarp and sand smelt. Preference for bottom
positions can be linked to feeding behaviour. For example, it has been shown
that Andalusian toothcarp’s ‘sister’ species, Aphanius iberus (Valenciennes), has
a diet based mainly on benthic crustaceans (Vargas & de Sostoa, 1997). Rincon
et al. (2002) also noted in experimental conditions that A. iberus tended to
occupy positions near the bottom of aquaria. These previous observations fit
well with toothcarp’s preference for positions near the stream bottom. Though
sand smelt is often considered a planktivorous species, it have been shown to be
an opportunistic feeder, switching to benthic prey when zooplankton is not
available (Vizzini & Mazzola, 2002). It is probable, therefore, that in stream
environments where, as far as is known the diet of sand smelt has never been
studied, the species would feed preferentially on benthic organisms.
On the other hand, predation risk could also limit the use of surface positions
by toothcarp and sand smelt, since in this situation fishes would be more
vulnerable to avian predators like egrets and kingfishers. As birds are sizeselective predators preferentially consuming larger fishes (Britton & Moser,
1982), the increased predation risk in surface positions could account for the
smaller size of toothcarps and sand smelts occupying them. Also, since egrets
and kingfishers are exclusively diurnal predators, the release of bird predation
pressure at night would allow larger toothcarps to move to the surface.
D E P T H A ND
R E FU G E
The results presented here show that the three studied species select microhabitat as a function of depth and presence of refuge, and that these preferences
vary with fish size and time of day. In general, the three species changed depth
preferences towards deeper areas at different stages during ontogeny, as has been
recorded in other fishes (Mallet et al., 2000; Rosenberger & Angermeier, 2003).
These spatial segregations of size classes can at the same time reduce intraspecific
competition (Heggenes, 1988) as well as reduce predation risk from a combination of aquatic and terrestrial predators (Power, 1984, 1987). Depth preferences
were stronger during daytime than at night in most species and size classes
(Fig. 3), suggesting that the diurnal bird predation could be an important factor
causing the observed depth preference patterns (Schlosser, 1988).
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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
Refuge (vegetation or other structures) can be an effective protection for fishes
both from terrestrial (Valdimarsson & Metcalfe, 1998) and from aquatic predators (Orth et al., 1984; Gotceitas, 1990). The responses of prey fishes in
relation to these two types of predation should be different, however, since
piscivorous fishes are gape-limited (Nilsson & Bronmark, 2000) and birds are
size-selective predators (Britton & Moser, 1982). Among the studied species
there was a stronger selection of depths than that observed for refuge, since
only size III toothcarps and size II sand smelts showed significant preferences
related to the presence of refuge (Table I). In the presence of refuge small
toothcarp and size II loach, however, occupied preferentially deeper microhabitats than in exposed areas. The presence of refuge also had a strong influence in
the depth-size structure of toothcarp and loach populations (Fig. 4).
During the day, the loach population had a strong depth-size structure, with
no size differences recorded between refuge and exposed microhabitats, while at
night toothcarp were smaller and did not follow the larger fish-deeper water
pattern in refuge microhabitats. As a cryptic and benthic species, loach is
probably less vulnerable to visual predators, such as birds and diurnal piscivorous fishes (Armbruster & Page, 1996). But loach can be also especially vulnerable to predation by eels, a species that, when feeding on fishes, feeds mainly
upon benthic species (Barak & Mason, 1992). Eels remain inactive in sheltered
habitats during daytime and forage at night (Baras et al., 1998; Schulze et al.,
2004). Predation risk due to eel activity is probably linked with the differences in
loach size between refuge and exposed habitat observed at night.
Toothcarp were larger in deeper microhabitats and at the same time smaller in
refuge than in exposed microhabitats during the day, but at night there was no
size-depth relation for toothcarp in refuge microhabitat. The diurnal pattern
seems to be influenced by an aquatic gape-limited predator, as refuge is occupied
by smaller individuals. But since eels are nocturnal, what is that diurnal aquatic
predator? One possibility is that small toothcarp are seeking refuge from viperine
snakes. Snakes are not truly gape-limited predators, but the higher energetic cost
of capturing large prey cause a positive selection of smaller or medium-sized prey
(Mehta, 2003; Moore et al., 2004). Another possibility is that some of the
invertebrate-feeding fish species occupying the stream stretch, mainly sand
smelt or flathead grey mullet M. cephalus, would be consuming small fishes. In
fact, some authors (Rosecchi & Crivelli, 1992; Bartulovic et al., 2004) have found
that fish larvae or juveniles are occasional prey of sand smelt, which is therefore
capable of becoming a small fish predator in certain conditions.
At night the presence of the otter in the study stretch, being nocturnal
predator (Beja, 1996) frequently consuming eels (Clavero et al., 2004), probably
preclude larger eels from occupying shallow areas. This predator exclusion could
be linked to the nocturnal maintenance of the size-depth relation in exposed
microhabitats observed in both toothcarp and loach (Fig. 4).
CO-OCCURRENC E
Results from the PCA showed that some of the patterns on the co-occurrence
of species and size classes could be related to differential habitat use (PC1 and
PC4). The PCA also showed clear segregations between toothcarp and sand
#
2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67 (Supplement B), 72–85
smelt (PC2) and between toothcarp and loach (PC3), however, which could not
be linked to any microhabitat characteristic. These observations suggest that
toothcarp tends to occupy microhabitats that are not being simultaneously used
by the other two species. One possible explanation for this pattern would be that
toothcarp excludes other small fishes through aggressive interactions. Aphanius
toothcarps, especially male individuals, have been shown to display aggressive
behaviours (Rincon et al., 2002). During the fieldwork male toothcarps were
seen defending territories by chasing and nipping other individuals (unpubl.
data). These aggressive interactions, however, were mainly directed to conspecifics, and would hardly explain the exclusion of loach and sand smelt.
The spatio-temporal segregation between toothcarp and both loach and sand
smelt could be also produced by a higher incidence of interspecific interactions
on toothcarp’s microhabitat use. Some cyprinodontid species in North America
have been shown to be very sensitive to interspecific interactions (Echelle et al.,
1972), often occupying harsh environments where they lack competitors and
major aquatic predators (McMahon & Tash, 1988). Iberian Aphanius species are
also very sensitive to the presence of other fish species, both native and introduced (Rincon et al., 2002; Prenda et al., 2003), and the most numerous
Andalusian toothcarp populations occupy hypersaline streams where there are
no other fish species (Doadrio et al., 2002). Being a critically endangered species,
the possible influences of these interactions on toothcarp populations should be
further investigated. To do so, the results presented here, which are from a
diverse fish community and the first available on the species’ microhabitat,
should be compared with locations where toothcarp do not coexist with any
other fishes.
We greatly acknowledge the assistance and company during the field work provided by
L. Fernandez, M. Narvaez, L. Barrios, J. Alvarez, E. Deuan, L. Dominguez and E. Perez.
Two anonymous referees made very useful comments on an early version of this work.
This study is part of the project ‘Biotic integrity and environmental factors of watersheds
in south-western Spain. Application to the management and conservation of
Mediterranean streams’ (Ministerio de Ciencia y Tecnologıa, REN2002–03513/HID)
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