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Animal Conservation. Print ISSN 1367-9430
Effect of salmonid introduction and other environmental
characteristics on amphibian distribution and abundance in
mountain lakes of northern Spain
G. Orizaola & F. Braña
Departamento de Biologı́a de Organismos y Sistemas, Universidad de Oviedo, Spain
Keywords
amphibian decline; introduced species;
predation.
Correspondence
Germán Orizaola. Current address:
Department of Ecology and Evolution/
Population Biology, Evolutionary Biology
Centre, Uppsala University, Norbyvägen
18D, SE-75 236 Uppsala, Sweden.
Tel: +46 18 4712688;
Fax: +46 18 4716424
Email: [email protected]
Received 1 March 2005; resubmitted
5 October 2005; accepted 18 November
2005
doi:10.1111/j.1469-1795.2006.00023.x
Abstract
Amphibians are currently experiencing a severe worldwide decline. Several factors,
such as habitat alteration, climate change, emerging diseases or the introduction
of exotic species, have been signalled as being responsible for the reduction of
amphibian populations. Among these, the introduction of fish predators has been
repeatedly indicated as a factor affecting the distribution of many species. The
present study was developed to examine the effect of fish presence and other
environmental factors on the distribution and abundance of amphibian species in
mountain lakes of the Cantabrian Range in northern Spain. We found no effect of
salmonid presence on the distribution and abundance of two widespread anuran
species Bufo bufo and Alytes obstetricans, whereas Rana temporaria showed a nonsignificant tendency to be absent from salmonid-occupied lakes. However, the
presence of introduced salmonids was the main negative factor explaining the
distribution of the newt species Triturus helveticus, Triturus alpestris and Triturus
marmoratus. The effect on these species is likely to be due to increased larval
mortality, as adult and egg predation by fish, or oviposition avoidance by female
newts has rarely been recorded. Fish removal and the creation of alternative
breeding habitats for amphibians are proposed as conservation measures to
recover amphibian populations in the vicinity of fish-stocked lakes.
Introduction
In recent years, amphibians have been the focus of important conservation efforts owing to severe population reductions and even extinction in many species (Houlahan et al.,
2000; Stuart et al., 2004; Beebee & Griffiths, 2005). The
causes of these declines are complex and sometimes difficult
to identify as they are reported to occur in very different
parts of the world, including pristine habitats (Alford &
Richards, 1999). Habitat destruction, water pollution, climate change, emerging diseases or introduced species have
been identified as factors most often affecting amphibian
populations (Collins & Storfer, 2003; Beebee & Griffiths,
2005). Interactions between these factors may create new
environmental pressures that lead to further severe reductions of amphibian populations (Kiesecker, Blaustein &
Belden, 2001). The study of the environmental variables that
influence the distribution of amphibian species in the wild
can contribute to a better understanding of the impact that
factors of anthropogenic origin can have on amphibian
populations, allowing us to distinguish between natural and
non-natural phenomena influencing amphibian distribution.
Amphibian species are exposed to a great variety of
breeding habitats, ranging from permanent lakes to tempor-
ary ponds, where predation and desiccation are the main
mortality factors (Wellborn, Skelly & Werner, 1996; Leips,
McManus & Travis, 2000; Babbitt, Baber & Tarr, 2003).
Pond desiccation is highly unpredictable and causes neartotal breeding failure during periods of drought. Predation
pressure is more consistent between years and so has a
relatively constant impact on amphibian assemblages (Wilbur, 1980; Alford, 1999). Among the different habitats that
amphibians occupy for breeding, mountain lakes represent
permanent localities that are often isolated from neighbouring river basins and that have limited predator communities,
commonly lacking top predators such as fish (e.g. Bahls,
1992 for western North America). Amphibians that are able
to occupy a broad range of habitats (see Van Buskirk, 2003)
can use lakes as refuges during dry seasons; the lakes
provide a source of individuals for immigration to neighbouring areas after a period of drought. Large permanent
water bodies can therefore be considered as hot spots for the
conservation of amphibian assemblages in mountain areas.
Mountain lakes present considerable variation in characteristics such as water volume, shore structure, vegetation
cover, refuge availability and type of substrate, which can
contribute towards explaining the patterns of variation in
amphibian abundance and distribution, and the great
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178 171
Effect of salmonid introduction on mountain amphibians
variation in species composition among lakes. One of the
main factors affecting amphibian assemblages in mountain
lakes is the introduction of exotic predators (Collins &
Storfer, 2003). In particular, the introduction of predatory
fish as a plague control agent or for recreational purposes
has been reported to cause severe declines in many natural
amphibian populations (Bradford, 1989; Brönmark & Edenhamn, 1994; Braña, Frechilla & Orizaola, 1996; Hecnar &
M’Closkey, 1997; Knapp & Matthews, 2000; Denoël,
Dzukic & Kalezic, 2005). Reduction of amphibian presence
in an area occupied by fish predators can be because of
either predator avoidance behaviours (mainly selective oviposition avoidance; see Resetarits & Wilbur, 1989; Hopey &
Petranka, 1994; Binckley & Resetarits, 2002) or direct
consumption (Gamradt & Kats, 1996; Laurila & Aho,
1997; Tyler et al., 1998; Binckley & Resetarits, 2002). The
impact of fish predators may be increased by the fact that
distances among mountain lakes are frequently outside
amphibian dispersal capacities (e.g. Jehle & Arntzen, 2000;
Holenweg, 2001; Schabetsberger et al., 2004), which can
prevent recolonization displacements (see e.g. Bradford,
Tabatabai & Graber, 1993).
This study evaluates the environmental correlates of
amphibian distribution and abundance in lakes of the
Cantabrian Mountains (northern Spain), and the effects that
introduced salmonid fish have on amphibian species. Some
lakes of the area are occupied by several salmonid and
cyprinid species (Braña et al., 1996). We have focused on
salmonid fish because they are one of the vertebrate groups
exerting a stronger predation pressure in permanent lakes
(e.g. Bradford, 1989; Resetarits, 1997; Tyler et al., 1998;
Gillespie, 2001; Matthews et al., 2001; Pilliod & Peterson,
2001; Knapp, 2005), whereas most cyprinids are partially
herbivorous or feed on small aquatic invertebrates and seem
to have a less important predatory capacity (Hecnar &
M’Closkey, 1997). The introduction of salmonids into ‘fishless’ lakes in the study area has previously been recorded to
have affected amphibians, as reported by Terrero (1951). He
described intense consumption of newts by introduced trout,
which was associated with a rapid decline of these amphibians. A preliminary study carried out in a few lakes in the
area also reported a reduction of amphibian distribution
associated with the presence of introduced predatory fish
(Braña et al., 1996). In this study, we considered both anuran
and urodele species and used the six most abundant species
(common toad Bufo bufo, common frog Rana temporaria,
midwife toad Alytes obstetricans, marbled newt Triturus
marmoratus, alpine newt Triturus alpestris and palmate newt
Triturus helveticus) to further analyse the influence of habitat
characteristics on amphibian presence and abundance.
Materials and methods
Habitat characterization
The study area is located in the central sector of the
Cantabrian Mountains, which runs along the north coast
172
G. Orizaola and F. Braña
of Spain for c. 480 km, rising to maximum altitudes of
2600 m. Field studies were conducted in a 5900 km2 area,
where 30 lentic permanent water bodies were selected to
provide a wide sample of lakes and ponds varying in
environmental characteristics (Supplementary Material Appendix S1). The study period extended from late May to
mid-July in 1998 and covered the larval developmental
period of all the amphibian species inhabiting these mountain areas (G. Orizaola & F. Braña, pers. data). The water
bodies considered in this study were naturally unoccupied
by fish (except for two lakes, Lillo and Embalse del Valle, for
which a natural origin of Salmo trutta is possible). However,
some of the lakes have been historically stocked with fish to
provide recreational angling. Several field and laboratory
measures were recorded to describe the physical, chemical
and biological characteristics of each lake. Lake elevation
(ALT) was obtained from 1:25 000 topographic maps (Instituto Geográfico Nacional), and perimeter (PER) and
maximum depth (DEP) were obtained from Fernández &
Garcı́a (1987). Shore slope (SLO), in degrees, was estimated
considering the distance from the shore to the point at
0.50 m in depth. Water temperature (TEM) was measured
at 0.50 m depth using a digital thermometer. Acidity (pH)
was measured by reflectometric methods (Reflectoquants,
Merck, Darmstadt, Germany, and RQflex 2 scanner). The
concentration of suspended matter (SMA) was determined
in 1 l samples, filtered using 47-mm-diameter Whatman
(Maidstone, England, UK) GF/A filters, which were subsequently dried at 50 1C for 24 h to obtain dry weight to the
nearest 0.0001 g. Per cent surface occupied by aquatic
vegetation growing in the lakeshore (VEG) was visually
estimated by two observers examining a strip of 5 m of the
lake shore; the mean value of both estimates was used for
analyses. Plankton abundance (PLA), expressed as individuals/litre, was obtained by filtering 1 l samples through a
53-mm mesh. Samples were preserved in formaldehyde
(10%) until analysis in the laboratory. All the measures
and samples were taken in five evenly distributed points of
each lake and averaged for analysis. Lake isolation (ISO)
was estimated by the straight-line distance to the nearest
permanent lake on 1:25 000 maps.
Fish and amphibian surveys
Data on fish presence/absence and species composition were
obtained by means of visual surveys, communication with
local fisheries authorities and from previous surveys involving electrofishing and gillnet catching (Braña et al., 1996).
Amphibian presence was determined by visual detection of
eggs, adults or larvae, by removal of rocks on the shore and
adjacent terrestrial habitats and by dip-netting surveys on
the entire shoreline. As amphibian breeding activity depends
on temperature and lake freezing and starts early in lower,
warmer areas (e.g. Laurila, Kartunen & Merilä, 2002;
Laugen, Laurila & Merilä, 2003), the surveys were scheduled to follow the elevation gradient, from lowest to highest
places. This procedure should be considered reliable, as
surveys conducted in the following years did not detect any
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178 G. Orizaola and F. Braña
Effect of salmonid introduction on mountain amphibians
(a)
Statistical analyses
(b) 100
90
80
Salmonids
No salmonids
70
60
50
40
30
20
10
0
B. bufo
n=17
Percentage of lakes with urodeles
Stepwise logistic regression analyses were used to evaluate
the effect of habitat characteristics on lake occupation by
the six most frequent amphibian species. In order to fit the
standard procedures of logistic regression analyses (see
Harrell, 2001), we first performed a principal component
analysis (PCA) to reduce the number of variables to be
included in the analysis. By means of PCA, we transformed
nine lake descriptors (ALT, PER, DEP, SLO, pH, TEM,
SMA, VEG and PLA) into compound variables, using the
scores from the significant PC axes for each lake in logistic
regression analyses. Salmonid fish presence/absence and
lake isolation were also included in the logistic regression
analyses as independent variables. The effect of environmental characteristics on salmonid fish occurrence was
analysed using the same procedures, using lake characteristics (PC axes) and ISO as factors. The effect of salmonid
predators on amphibian abundance was investigated by
means of Mann–Whitney tests. The level of significance
was set at a = 0.05 for all tests.
Percentage of lakes with anurans
new amphibian species in the lakes. Besides, larvae of the
studied species remain in the water for several weeks or even
months, so the risk of having false-negative records should
be minimum. Amphibian abundance was estimated as the
average number of individuals (adult and larvae) hand
netted by two people during 5-min exhaustive sampling in
five points of the lake (the same points where habitat
parameters were recorded). The same two people surveyed
all the lakes. All the surveys were conducted in a short
period of time (6 weeks), at the same time of the day and
always following the elevation gradient described previously. Adult anurans were not included in abundance
analyses as they were captured only in small numbers.
A. obstetricans R. temporaria R. perezi
n=14
n =15
n =4
90
Salmonids
No salmonids
80
70
60
50
40
30
20
10
0
T. marmoratus T. alpestris T. helveticus
n=8
n=13
n =21
T. boscai S. salamandra
n =3
n =5
Figure 1 Amphibian distribution (all stages considered) in lakes with or
without the presence of fish predators. The total number of lakes
where each species was found is indicated. (a) Anurans, (b) urodeles.
Table 1 Loading of the lake variables on the two first factors extracted
by the principal components analysis (PC1 and PC2)
PC1
Results
Five anuran and five urodele species were detected in the
surveys, the common toad B. bufo, common frog R. temporaria and midwife frog A. obstetricans being the most
frequent anurans (Fig. 1a), and palmate newt T. helveticus,
alpine newt T. alpestris and marbled newt T. marmoratus
being the most frequent urodeles (Fig. 1b). All these species
are commonly found in northern Spain, occupying a broad
range of habitats from temporary ponds to larger lakes
(Barbadillo et al., 1999; Van Buskirk, 2003). Seven fish
species were detected in the surveyed lakes (salmonids:
brown trout S. trutta, rainbow trout Oncorhynchus mykiss
and brook trout Salvelinus fontinalis; non-salmonids: minnow Phoxinus phoxinus, tench Tinca tinca, carp Cyprinus
carpio and Iberian roach Chondrostoma arcasii; Supplementary Material Appendix S1). The results of the PCA conducted on group lake descriptors showed a first axis (PC1)
that explained 28% of the total variance of lake characteristics and a second one (PC2) that explained 19% (Table 1).
Four variables loaded significantly in the first axis: PER,
DEP and SLO with a negative sign and PLA with a positive
H. arborea
n=1
Altitude
Perimeter
Depth
Shore slope
Water temperature (0.5 m)
pH
Suspended matter
Shoreline vegetation cover
Plankton abundance
Explained variance
0.211
0.703
0.725
0.730
0.089
0.039
0.635
0.514
0.739
2.822
PC2
0.601
0.488
0.365
0.021
0.678
0.723
0.325
0.314
0.252
1.983
Significant at a= 0.05.
sign. In the second axis, only pH loaded significantly, with a
negative sign (Table 1).
Eight out of 30 lakes, mainly comparatively deep, with a
large perimeter, steep shore slope and low plankton abundance, contained predatory fish (Table 2, Supplementary
Material Appendix S1). Analyses on habitat variables
showed that B. bufo distribution was influenced by lake
characteristics (PC1, Table 2), being more frequently found
in deep lakes with a large perimeter and steep slope, as well
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178 173
Effect of salmonid introduction on mountain amphibians
G. Orizaola and F. Braña
Table 2 Results of logistic regression analyses for the presence of salmonids and each amphibian species
Salmonids
PC1
PC2
ISO
Coefficient
Direction
of effect Coefficient P
Direction
of effect Coefficient P
Direction
of effect Coefficient P
Salmonid fish
–
Bufo bufo
1.493
Alytes obstetricans 0.049
Rana temporaria
2.727
Triturus helveticus 13.032
T. alpestris
5.117
T. marmoratus
3.967
P
–
0.222
0.825
0.099
o0.001
0.024
0.046
–
NE
NE
NE
7.855
9.845
0.316
1.714
7.130
2.294
6.879
0.005
0.002
0.574
0.191
0.008
0.130
0.009
7.613
2.414
1.899
1.534
0.334
1.068
0.011
NE
NE
+
NE
+
0.006
0.120
0.168
0.216
0.563
0.301
0.916
NE
NE
NE
NE
NE
NE
0.249
3.294
8.195
2.561
2.188
0.515
0.095
Direction
of effect
0.618
0.070
0.004
0.110
0.139
0.473
0.758
NE
NE
+
NE
NE
NE
NE
as in areas with low plankton density (Supplementary
Material Appendix S1). In the case of A. obstetricans, the
distribution was mainly influenced by lake isolation (Table
2), being preferentially found in lakes far apart from other
permanent lakes (Supplementary Material Appendix S1).
The distribution of R. temporaria was not significantly
affected by any of the considered factors (Table 2), despite
showing a tendency to be absent from salmonid-occupied
lakes (only two salmonid lakes had R. temporaria, Fig. 1a).
The presence of salmonid fish did not affect the distribution
(Table 2) and abundance of B. bufo, A. obstetricans and
R. temporaria (U22,8 = 69.5, P= 0.365; U22,8 = 79.5,
P= 0.665; and U22,8 =59.5, P= 0.146, respectively; Fig. 2).
The presence of salmonid fish in mountain lakes was
strongly associated with the absence of urodeles (Table 2,
Fig. 1b). Considering altogether the three most frequent
species (T. helveticus, T. alpestris and T. marmoratus), both
larvae and adult abundance were negatively affected by
salmonid presence (U22,8 = 32, P= 0.004 for larvae and
U22,8 = 39.5, P= 0.019 for adults, Fig. 2). The distribution
of T. helveticus and T. marmoratus, and to a lesser extent
T. alpestris, was also correlated with lake characteristics
(PC1, Table 2), these species being preferentially found in
lakes with low perimeter, depth and slope and high plankton
abundance (Supplementary Material Appendix S1).
Discussion
As permanent habitats, mountain lakes provide a crucial
environment for amphibian reproduction, especially during
dry summers when reproduction can fail in adjacent temporal habitats because of desiccation (Pilliod, 2001). Lakes
stocked with salmonids may act as sink habitats for amphibians, as predation can reduce the number of individuals
that reach metamorphosis and can consequently produce
recruitment failure (Pilliod & Peterson, 2001). The effect of
fish introductions could be increased as a consequence of the
high fidelity in oviposition site selection shown by some
amphibian species (Berven & Grudzien, 1990; Laurila &
Aho, 1997). The results of the present study indicate that the
presence of salmonid fish is the main factor explaining the
174
Amphibian abundance (individuals/survey)
Salmonid presence (for amphibian presence), principal components 1 and 2 and lake isolation were used as predictor variables. Regression
coefficients, P-values and the direction of the effect are given. Codification of environmental variables is explained in the Materials and methods.
NE, no effect.
80
Salmonids
No salmonids
70
60
50
40
20
10
0
Bufo
Alytes
Rana
Adult
newts
Larvae
newts
Figure 2 Abundance of amphibians (mean number 1 SE) in lakes
with or without fish predators. Anuran abundance represents only
larval abundance.
species richness and the composition of amphibian communities in mountain lakes of northern Spain. Salmonids were
found in comparatively deep lakes with large perimeters and
high shore slopes, characteristics associated with the large
water volume necessary to maintain physiological and feeding requirements of large fish. Amphibian diversity and
abundance were considerably reduced in this type of lake.
The results obtained in this work are similar to those of
previous studies, reaffirming the crucial role that fish introductions could exert at the local level on native amphibian
fauna (Bradford, 1989; Bradford et al., 1993; Brönmark &
Edenhamn, 1994; Hecnar & M’Closkey, 1997; Tyler et al.,
1998; Knapp & Matthews, 2000; Gillespie, 2001; Pilliod &
Peterson, 2001; Hamer, Lane & Mahony, 2002).
The impact of salmonid fish was, however, notably
different depending on the amphibian species. Bufo bufo
inhabits most lakes stocked with salmonids, where high
larval densities are present. This could be related to the
presence of highly toxic compounds (bufotoxins) in the skin
of adults and larvae of this species, effective against vertebrate predators (Denton & Beebee, 1991; Crossland
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178 G. Orizaola and F. Braña
& Alford, 1998; Benard & Fordyce, 2003). However,
the effects of salmonid presence on A. obstetricans and
R. temporaria seem far more complex. Alytes obstetricans
did not appear to be strongly affected by the presence of
salmonids (it was detected in about half of the lakes
occupied by salmonids), although larvae density was lower
in lakes occupied by these predators. The mechanisms that
allow A. obstetricans to coexist with fish predators are
unclear; nevertheless, this species shows several life-history
characteristics that could contribute to a tolerance to
salmonid fish. For example, larvae of this species hatch at
an advanced developmental stage and with a large size
(Márquez, 1996), characteristics associated with high escape
capabilities and low larvae mortality because of predation
(Cronin & Travis, 1986; Richards & Bull, 1990). Alytes
obstetricans larvae were also located hiding in the vegetation
more frequently than other amphibian species, which could
increase their survival. The difference in our results from
those reported for Central Spain, where A. obstetricans
apparently fails to reproduce in favourable areas when these
are occupied by fish predators (S. fontinalis; Martı́nezSolano, Barbadillo & Lapeña, 2003), suggests that differences in habitat structure could be responsible for a differential impact of fish predators. In the case of R. temporaria,
a lower survival was reported for larvae exposed to predatory fish (Laurila & Aho, 1997; Laurila, 1998), which
could be associated with the disappearance of frogs from
lakes stocked with predatory fish. This agrees with the
findings of other studies reporting a negative spatial correlation between predatory fish and different Rana species
(Bradford, 1989; Bradford et al., 1993; Knapp & Matthews,
2000; Knapp, Matthews & Sarnelle, 2001; Pilliod & Peterson, 2001). In our study, R. temporaria showed a nonsignificant tendency to be affected by the presence of
salmonid fish in the surveyed lakes, being absent from the
majority of lakes stocked with predatory salmonid fish.
Urodeles seemed to be more severely affected by the
presence of salmonid fish than anurans, as introduced
salmonids significantly affected the distribution and abundance of all the Triturus species considered in the analyses.
Newts were restricted almost exclusively to salmonid-free
lakes and newt larva was not detected in salmonid-occupied
lakes. Especially remarkable is the case of T. marmoratus,
which was not found in lakes with salmonids, supporting the
results found in Switzerland for T. cristatus, a closely related
species (Van Buskirk, 2005). In this sense, a report at the
time of first salmonid introductions signalled a high consumption of adult newts by introduced trout on several of
the studied lakes (Terrero, 1951). This report confirms the
previous suitability of these lakes for newt reproduction, as
well as the impact that salmonid introductions have had on
this group, which is currently almost absent from lakes
containing introduced salmonids. Similar negative effects
of fish presence have been reported for Triturus and other
urodele species worldwide (Petranka, 1983; Beebee, 1985;
Semlitsch, 1988; Ildos & Ancona, 1994; Aronsson & Stenson, 1995; Gamradt & Kats, 1996; Hecnar & M’Closkey,
1997; Tyler et al., 1998; Smith et al., 1999; Barr & Babbitt,
Effect of salmonid introduction on mountain amphibians
2002). In addition to direct predation on any life-history
stage, the current distribution of amphibian species could
also be explained by the avoidance of unsuitable (because of
high predation risk) oviposition places. Avoidance of fishoccupied habitats for oviposition has been reported for
several urodele species (Kats & Sih, 1992; Gamradt & Kats,
1996). However, recent studies on newt oviposition behaviour have shown that Triturus species do not alter
their oviposition site selection in response to fish presence
(Orizaola & Braña, 2003, except for T. marmoratus), and
neither does R. temporaria (Laurila & Aho, 1997). Otherwise, larvae of many amphibian species are usual prey of fish
(e.g. Kats, Petranka & Sih, 1988; Denton & Beebee, 1991),
whereas predation on egg or adult stages of amphibians has
been reported less frequently (Wilbur, 1980; Kats & Ferrer,
2003), which could indicate that the main impact of fish
predation should operate at the larval stage.
Fish introductions, and more widely the introduction of
exotic competitors and predators, have been reported as one
of the main causes responsible for the observed global
amphibian decline (Bradford, 1989; Wake, 1991; Brönmark
& Edenhamn, 1994; Braña et al., 1996; Knapp & Matthews,
2000; Gillespie, 2001; Hamer et al., 2002; Kats & Ferrer,
2003). The results of the present study show that salmonid
fish presence differentially affects various amphibian species, altering the composition of the amphibian community
and reducing its richness in mountain lakes of Northern
Spain. In this area, lakes without salmonids hold comparatively diverse amphibian communities with up to six species
frequently coexisting, whereas in lakes stocked with predatory salmonids B. bufo and, to a lesser extent, A. obstetricans
are almost the only species present, Triturus sp. and Rana sp.
being virtually absent. In the light of these results, conservation measures are necessary for the maintenance of amphibian populations in these lakes. Fish eradication
would obviously be the most effective, but would probably
be only feasible in small lakes isolated from any fish population source (Knapp & Matthews, 1998). For this purpose,
application of piscicides (e.g. rotenone, antimycin) is unsuitable because of their great impact on local native fauna
(Aronsson & Stenson, 1995; Knapp & Matthews, 1998).
Considering the high fidelity of amphibian species to their
breeding localities, another way to recover natural amphibian populations could be the creation of alternative permanent habitats for amphibian reproduction in the proximity
of fish-occupied lakes, which could be used by a great
variety of species without the risk of being preyed by fish.
These methods would likely be effective given the apparent
great resistance and resilience of amphibian fauna to fish
introductions, as proven by the recoveries of R. muscosa,
Ambystoma macrodactylum and Ambystoma gracile populations soon after trout eradication in mountain lakes (Funk
& Dunlap, 1999; Knapp et al., 2001; Hoffman, Larson &
Samora, 2004; Vredenburg, 2004). Preventing new introductions and immediate eradication of recently introduced fish
should be the most effective management measures to assure
the preservation of amphibian populations in lakes naturally unoccupied by predatory fish.
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178 175
Effect of salmonid introduction on mountain amphibians
Acknowledgements
We are especially grateful to Carlos Rodrı́guez del Valle for
the invaluable assistance in the fieldwork and to Felipe G.
Reyes-Gavilán for the critical comments on the manuscript.
Surveys were conducted with the permission of the Picos de
Europa National Park, Somiedo Natural Park and the
regional authorities (Dirección General de Recursos Naturales y Protección Ambiental del Principado de Asturias).
A Spanish Ministry of Education and Culture doctoral
fellowship and a University of Oviedo research contract to
G. Orizaola supported this research.
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Supplementary material
The following material is available for this article online:
Appendix S1 Physical and biological characteristics of
the surveyed lakes.
This material is available as part of the online article
from http://www.blackwell-synergy.com
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 171–178