Content uploaded by Francisco Javier Diego-Rasilla
Author content
All content in this area was uploaded by Francisco Javier Diego-Rasilla
Content may be subject to copyright.
ORIGINAL PAPER
Acoustic orientation in the palmate newt,
Lissotriton helveticus
Francisco J. Diego-Rasilla &Rosa M. Luengo
Received: 11 February 2006 /Revised: 18 November 2006 / Accepted: 13 January 2007 / Published online: 22 February 2007
#Springer-Verlag 2007
Abstract Experiments reported here were carried out to
investigate the use of acoustic cues by palmate newts
(Lissotriton helveticus) for orientation and to study whether
this behavior is learned, or whether two populations of
palmate newts that cohabit with different frog species
(Iberian green frog, Rana perezi, and European common
brown frog, Rana temporaria) show different phonotactic
preferences. The orientation tests consisted of presenting a
control stimulus (white noise), a sympatric acoustic
stimulus (calls of R. perezi or R. temporaria, depending
on the origin of newts), or an allopatric stimulus (calls of
natterjack toads, Bufo calamita,orR. perezi). Newts were
released in a circular arena, while the acoustic stimuli were
presented outside of the circular arena in four different
compass orientation directions (0, 90, 180 and 270°). In this
study, we show that L. helveticus performed positive
phonotaxis toward the calls of R. perezi only when both
species shared habitat, orienting randomly when R. perezi
was absent from the newt’s natal population. Newts from
both populations oriented randomly when exposed to the
allopatric and control acoustic stimuli. These results
suggest, for the first time, that recognition of the sympatric
heterospecific calls could be learned. However, newts
sharing the breeding pond with a population of R.
temporaria oriented randomly when exposed to the calls
of this species. The fact that the breeding seasons of R.
temporaria and L. helveticus do not overlap in time does
not allow the use of R. temporaria calls as a guidance
mechanism for migrating individuals of L. helveticus.
Keywords Acoustic orientation .Homing .Migration .
Phonotaxis .Newt
Introduction
Homing ability has been documented in different species of
newts (e.g., Taricha rivularis: Twitty et al. 1966;Notoph-
thalmus viridescens: Phillips 1987; Phillips et al. 1995;
Triturus marmoratus: Diego-Rasilla and Luengo 2002;
Mesotriton alpestris: Joly and Miaud 1989; Diego-Rasilla
2003; Diego-Rasilla et al. 2005), and several cues have
been shown to play a role in their homing orientation.
Newts may be capable of homing using celestial (Landreth
and Ferguson 1967; Diego-Rasilla and Luengo 2002) and
magnetic cues (Phillips 1986; Fischer et al. 2001; Diego-
Rasilla 2003,2004; Diego-Rasilla et al. 2005). Also, it has
been found that odors from ponds (Joly and Miaud 1993)
and acoustic cues (Diego-Rasilla and Luengo 2004) may be
stimuli involved in orientation responses, improving the
accuracy of orientation during the final approach to the
breeding pond.
The possible role of acoustic cues in orientation of newts
has received little attention. However, although newts do
not seem capable of acoustic communication (Wilczynski
and Ryan 1988), a recent study has found that T.
marmoratus shows heterospecific call recognition and
positive phonotaxis when exposed to the advertisement
Behav Ecol Sociobiol (2007) 61:1329–1335
DOI 10.1007/s00265-007-0363-9
Communicated by J. Christensen-Dalsgaard
F. J. Diego-Rasilla (*)
Departamento de Biología Animal, Universidad de Salamanca,
Campus Miguel de Unamuno, Edificio de Farmacia, 5
a
planta,
37007 Salamanca, Spain
e-mail: fjdiego@herpetologica.org
R. M. Luengo
Departamento de Prevención y Medioambiente, ENIAC,
C/ Caldereros 11,
37001 Salamanca, Spain
calls of anurans with which they share a breeding pond
(Diego-Rasilla and Luengo 2004).
Newts lack middle and external ears, but they have
inner ears that can process sound (Hetherington 2001).
Hetherington (2001) found that the lateral body wall and
lungs of newts may function in sound reception, especially
at relatively low frequencies (i.e., peak motion ranging
from 1,600 to 2,500 Hz) in small newts, as is the case in
palmate newts. Sound causes the newt’s lungs to vibrate,
and the vibrations are transmitted from the lungs to the
newt’s inner ear for processing.
Experiments reported here were carried out to character-
ize the use of acoustic cues by palmate newts (Lissotriton
helveticus) for orientation, addressing some of the questions
left open by our previous work (Diego-Rasilla and Luengo
2004), such as whether this behavior is learned, or whether
two populations of the same species that cohabit with dif-
ferent frog species show different phonotactic preferences.
Specifically, we studied the orientation responses of
palmate newts to the advertisement calls of natterjack toads
(Bufo calamita), of European common brown frogs (Rana
temporaria) and of Iberian green frogs (Rana perezi). We
hypothesized that newts would recognize the signals of a
sympatric species that would share habitat with them but
not those of a species that would be absent from natal
populations. Moreover, this capability might elicit positive
phonotaxis.
Materials and methods
Subjects and study site
Two groups of adult palmate newts were collected in 2005;
one group from a garden pond of 2 m
2
, situated in Barros
(Cantabria, northern Spain; 43°17′7″N, 4°4′41″W; 61 m
a.s.l.), and another group collected from a pond situated
in a mountainous area, at the Saja-Besaya Natural Park
(Cantabria, northern Spain; 43°13′51″N, 4°09′50″W;
382 m a.s.l.). Newts were collected by dip netting from
breeding ponds during the seasonal migratory periods. In
the lowland area, palmate newts begin their migration to
their breeding ponds in February, but large numbers of
newts have not been found in the ponds until late March.
However, in the mountainous area, their seasonal migra-
tory period usually extends from late March to early
May. Also, in both populations, the males are the first to
arrive at the ponds (personal observation). During July
or, even later, in August, the adult newts leave the water.
Palmate newts typically hibernate in deep leaf litter in
late September and no further than 150 m away from their
spring reproductive area. The young newts have more
terrestrial habits and show a high dispersal and coloniza-
tion capacity, covering distances up to a few kilometers
away from their birth area (Montori and Herrero 2004).
The two ponds were separated by 9.21 km. The garden
pond was artificially created in 12 October 2001, and it was
weekly monitored during the next 12 months to assess
colonization by amphibians. This pond is situated 290 m
away from the nearest aquatic habitat. The first amphibian
species arriving at the pond was R. perezi (17 March 2002),
followed by the appearance of L. helveticus 13 days later.
No other species of amphibians have been found to date at
the pond, although Bufo bufo and Alytes obstetricans have
been observed in the study area. The pond at the Saja-
Besaya Natural Park is used for breeding by three species
of urodeles (L. helveticus,Mesotriton alpestris and
Salamandra salamandra) and one anuran species (R.
temporaria), which is found in Spain mainly in mountain-
ous areas (Barbadillo et al. 1999).
Procedure
At the lowland site (Barros), 23 newts (9 adult males and
14 adult females) were captured in 2005 (6 May) between
1830 and 1900 hours (GMT). Sixteen newts (15 adult
males and 1 adult female) were captured between 1530 and
1700 hours (GMT) in 2005 (30 March) at Saja-Besaya.
Newts were placed in opaque plastic containers (54 × 35×
21 cm) in which the water depth was 1 cm and taken to the
indoor testing arena. Animals were tested between 2 and
9 h after being captured because they show the highest
levels of activity during the first hours of the night, and
their homing behavior takes place during the night (Montori
and Herrero 2004). They were returned to their pond just
after testing.
TestingprotocolsdescribedbyDiego-Rasillaand
Luengo (2004) were basically used. Newts were tested
indoors in an arena consisting of a circular plastic container
(45 cm diameter, 25 cm high). The floor and arena walls
were thoroughly wiped with a damp cloth between trials to
eliminate directional olfactory cues (Fischer et al. 2001),
and then, they were wiped dry using paper towels.
Just before their individual testing session, newts were
kept individually, and acoustically isolated, for 5 min in
opaque plastic containers (34×24×16 cm), containing
water from the newt’s home pond, in which the water
depth was 1 cm. For testing, a newt was removed
individually from its plastic container and put in the arena
center in complete darkness beneath an opaque, cylindrical
plastic container (9 cm diameter, 14.5 cm high) that served
as a release device. Then, we presented the acoustic
stimulus (see details below). Newts were held in the
container for 1 min to overcome the effects of handling
before the release device was lifted, allowing them to move
freely about the arena. To minimize disturbance during the
1330 Behav Ecol Sociobiol (2007) 61:1329–1335
experiments, the observers moved away from the arena,
leaving each animal undisturbed for 5 min. Individual trials
were discontinued, if the newt remained motionless in the
arena center for 5 min. The directional responses of each
newt that left the central area was recorded by the moist
trails that it left on the floor of the arena. In all cases, newts
that left the central area moved directly from their initial
position to the arena wall, tapped against the wall, and then
clinging to the wall, proceeded to circle around the arena.
Directional responses were recorded to 5° accuracy as the
vector of the first point where an animal made contact with
the wall.
We carried out two different experiments: (1) The first
experiment was performed using newts collected from Saja-
Besaya; in this experiment, the orientation tests consisted of
presenting a control stimulus (white noise), a sympatric
acoustic stimulus (the calls of R. temporaria), or an
allopatric stimulus, the calls of R. perezi. (2) The second
experiment was performed using newts collected from
Barros; the orientation tests consisted of presenting a
control stimulus (white noise), a sympatric acoustic
stimulus (the calls of R. perezi), or an allopatric stimulus
(the calls of B. calamita) that L. helveticus would not be
expected to recognize. L. helveticus and R. perezi occur in
sympatry in this lowland area, but B. calamita is not present
in the study area. Thus, B. calamita occurs over most of the
country, except the northern parts of the Iberian Peninsula
where we carried out these experiments (Reques and Tejedo
2002). The nearest populations of B. calamita are ∼30 km
away from Barros and ∼20 km away from Saja-Besaya
(Reques and Tejedo 2002).
The calls of R. perezi,R. temporaria and B. calamita
(Fig. 1; sample format 16-bit signed PCM [Pulse Code
Modulation], sample rate 48,000 Hz) were obtained from
Márquez and Mateu (1995) and were stored on a notebook
computer (MITAC 5033). The length of time for playback
sequences was 1 min, and they were played in continuous
loop mode. The calls of R. perezi and B. calamita represent
a small group of males (Fig. 1a,b), and the calls of R.
temporaria were from a pair of males (Fig. 1c; Márquez
Fig. 1 Spectrogram views of acoustic signals. aCalls of Rana perezi,
bcalls of Bufo calamita and ccalls of Rana temporaria. The
spectrogram view represents time on the horizontal axis, frequency on
the vertical axis in kHz and relative intensity at each time and
frequency as a grayscale value. All three spectrograms have the same
window type (Hann), window size (=512 samples, 10.7 ms), time grid
spacing = 5.8 ms (frame overlap = 50%), frequency grid spacing =
93.8 Hz (FFT size = 512 samples) and 3-dB bandwidth (=135 Hz)
Behav Ecol Sociobiol (2007) 61:1329–1335
and Mateu 1995). The calls were broadcast to subjects
using Tsunami EA-968 speakers (Tsunami, Guangdong,
China) and Cool Edit 96 acoustics software (Syntrillium
Software, Phoenix, USA). The overall absolute sound
pressure level (dB SPL) of the calls, measured 20 cm from
the speakers (i.e., the distance of the newt to the speakers)
with a Digital Sound Level Meter (Electro Tools ET 9901,
Guijarro Hermanos, Madrid, Spain), was 68 dB. This
corresponds to the sound level of R. perezi calls 10–12 m
from the breeding pond.
The acoustic stimuli were presented outside of the
circular arena in four different compass orientation direc-
tions (0, 90, 180 and 270°), being the speakers positioned
just below the lip of the arena. We randomized the order of
the stimulus presentation for each individual in each
experimental condition. In the first experiment, the first
four newts were tested with the allopatric acoustic stimulus
(i.e., the calls of R. perezi), followed by four fresh newts
tested with the sympatric acoustic stimulus (i.e., the calls of
R. temporaria) and four more newts tested with the control
acoustic stimulus (i.e., white noise). In the second exper-
iment, the first four newts were tested with the allopatric
acoustic stimulus (i.e., the calls of B. calamita), followed
by four fresh newts tested with the sympatric acoustic
stimulus (i.e., the calls of R. perezi) and four more newts
tested with the control acoustic stimulus (i.e., white noise).
In both experiments, newts tested with the allopatric,
sympatric and control acoustic stimuli were separately
placed in opaque plastic containers (54 × 35 × 21 cm) in
which the water depth was 1 cm. When all the newts had
been tested in one of three acoustic conditions, newts
previously tested with the allopatric acoustic stimulus were
tested with the sympatric acoustic stimulus; those previ-
ously tested with the sympatric acoustic stimulus were
tested with the control stimulus, and newts previously
tested with the control acoustic stimulus were tested with
the allopatric stimulus (this was again done in a random
order). In all the experiments, these sequences were
repeated until all the newts had been exposed once to the
sympatric acoustic stimulus, once to the allopatric stimulus
and once to the control stimulus. Also, in the first
experiment, the first individual was tested with the acoustic
stimulus from a 180° direction, the next individual was
tested with the stimulus from 0°, followed by one tested
with the stimulus from 90° and one tested with the stimulus
from 270°. The order of the four acoustic stimuli directions
was 270, 90, 180 and 0° in the second experiment. The
order of the four acoustic stimuli directions was determined
using a random number sequence. This sequence was
repeated until the test had been completed. If a newt did not
reach the orientation criterion within the appropriate time
interval, the next individual was tested with the stimulus
from the same direction. Accordingly, data pooled from an
entire test series included roughly equal numbers of
bearings from newts tested in each of the four symmetrical
orientation directions of the acoustic stimuli. Data from the
four conditions are combined by rotating the bearings so
that the acoustic stimuli compass directions coincide at 0°
(i.e., 90° is subtracted from the actual headings of newts
tested with the acoustic stimuli from 90°, 180° from the
headings of newts tested with acoustic stimuli from 180°,
and 270° from the headings of newts tested with acoustic
stimuli from 270°). Pooling the acoustic bearings from an
approximately equal number of newts tested in each of the
four acoustic stimuli directions made it possible to factor
out any consistent non-acoustic bias (Diego-Rasilla and
Luengo 2004).
Data were analyzed using standard circular statistics
(Batschelet 1981; Fisher 1995). The mean vector bearing
was calculated by vector addition and tested for signifi-
cance using a modified Rayleigh test, the Vtest. This test
was used to test closeness to expected orientation (i.e., the
direction of the acoustic stimuli, 0°), and the Watson U
2
test
was used to test for differences between distributions,
providing a criteria to test whether two samples differ
significantly from each other (Batschelet 1981; Mardia and
Jupp 2000).
Results
Experiment 1 (Saja-Besaya/highland experiment)
Newts were randomly oriented with respect to sound in all
of the three acoustic conditions: the calls of R. temporaria
(i.e., the sympatric acoustic stimulus; 46 ± 77°; Vtest with
expected direction = 0° r=0.25, N= 16, P= 0.16; Fig. 2a),
the calls of R. perezi (i.e., the allopatric acoustic stimulus;
49±73°; Vtest with expected direction = 0° r= 0.32, N= 15,
P=0.123; Fig. 2b) and the white noise (195 ± 99°; Vtest
with expected direction = 0° r= 0.23, N=11, P=0.845;
Fig. 2c). The distributions of the orientation data under the
three treatments are not significantly different (Watson U
2
test: NS in all cases; Fig. 2).
Experiment 2 (Barros/lowland experiment)
Newts tested with the sympatric acoustic stimulus (i.e., the
calls of R. perezi) were oriented towards the sound source
(34±42°; Vtest with expected direction = 0° r= 0.41, N=
19, P=0.017; Fig. 3a), whereas both the distribution of
bearings in the presence of the allopatric acoustic stimulus
(i.e., the calls of B. calamita; 14°; Vtest with expected
direction = 0° r=0.15, N= 15, P= 0.213; Fig. 3b), and the
distribution of headings in the presence of the control
acoustic stimulus (i.e., white noise; 78 ± 168°; Vtest with
1332 Behav Ecol Sociobiol (2007) 61:1329–1335
Fig. 2 Orientation responses of
the palmate newts from the
mountainous area (i.e., experi-
ment 1) ato the sympatric
acoustic stimulus (i.e., the calls
of European common brown
frogs), bto the allopatric acous-
tic stimulus (i.e., the calls of
Iberian green frogs) and cto the
white noise. Symbols indicate
the direction of movement of
each individual newt tested only
once in one of four symmetrical
acoustic stimuli orientation
directions (i.e., 0, 90, 180 and
270°). The location of speakers
broadcasting the calls is
referenced at 0°. The arrow at
the center of the diagram indi-
cates the mean direction of
orientation; the length of the
arrow is proportional to the
mean vector length (r). Dashed
lines indicate the 95% confi-
dence intervals for the mean
vector length; the radius of each
diagram corresponds to r=1
Fig. 3 Orientation responses of
the palmate newts breeding in
Barros (i.e., experiment 2) ato
the sympatric acoustic stimulus
(i.e., the calls of Iberian green
frogs), bto the allopatric stimu-
lus (i.e., the calls of natterjack
toads) and cto the white noise.
Symbols are the same as in
Fig. 2
Behav Ecol Sociobiol (2007) 61:1329–1335
expected direction = 0° r= 0.09, N= 23, P= 0.453; Fig. 3c)
were indistinguishable from random. The distributions of
the orientation data under the three treatments are not
significantly different (Watson U
2
test: NS in all cases;
Fig. 3).
Discussion
The present findings provide more evidence of heterospe-
cific call recognition and positive phonotactic response in
urodeles and show the role of acoustic cues as reference
cues for orientation by L. helveticus, as previously described
in T. marmoratus (Diego-Rasilla and Luengo 2004).
Palmate newts performed positive phonotaxis toward the
calls of the Iberian green frogs only when both species
shared habitat (i.e., lowland population), orienting ran-
domly when the Iberian green frogs were absent from the
newt’s natal population (i.e., the population of the moun-
tainous area). Also, newts from both populations oriented
randomly when exposed to the allopatric and control
acoustic stimuli. These findings support the hypothesis that
the newts are capable of recognizing the advertisement calls
of anurans with which they share a breeding pond (Diego-
Rasilla and Luengo 2004), although palmate newts sharing
the breeding pond with a population of European common
brown frogs (i.e., newts from the mountainous area) did not
show any orientation response when exposed to the calls of
this anuran species.
Breeding phenology by R. temporaria could explain why
their breeding calls did not elicit any orientation response.
This species is an explosive pond breeder (i.e., reproduces
in a very short time frame), and the breeding period is much
shorter in this species than in other species of frogs
(Elmberg 1990; Barbadillo et al. 1999; Nieto-Román et al.
2004). Also, R. temporaria usually breeds in our study area
in early February, although we have found some floating
clutches in early January (personal observation). However,
in this mountainous area, palmate newts usually begin their
migration to their breeding pond in late March, although
large numbers of newts have not been found in the ponds
until early May (personal observation). In reality, palmate
newts co-occur in the pond with tadpoles of R. temporaria
but not with adult frogs. Therefore, the fact that the
breeding seasons of R. temporaria and L. helveticus do
not overlap in time makes impossible the use of calls of
R. temporaria as a guidance mechanism for migrating
individuals of L. helveticus. Consequently, newts breeding
in the same pond as European common brown frogs did not
recognize their calls and oriented randomly when exposed
to the calls of frogs.
In L. helveticus and T. marmoratus (Diego-Rasilla and
Luengo 2004), we have found a lack of response to frog
breeding calls broadcast in regions uninhabited by the frog
species. The same breeding calls of natterjack toads were
recognized and elicited positive phonotaxis by marbled
newts (Diego-Rasilla and Luengo 2004), whereas palmate
newts were unable to use them for orientation because
natterjack toads are completely absent from our study area
(Reques and Tejedo 2002), and the palmate newts had
never heard the calls of this toad species. Our results
suggest that this orientation behavior seems to be a plastic
behavior pattern that can be adjusted to local conditions
and community composition. Thus, the same species, L.
helveticus, might use acoustic cues from different species
or no cue at all depending upon the location of their
breeding pond.
In some anuran species, like B. calamita (Sinsch 1990a,
1992a) and Bufo fowleri (Ferguson and Landreth 1966),
conspecific calls are useful for orientation but not indis-
pensable. Amphibians rely on a variety of orientation cues
to find their way around their home ranges or to locate
breeding ponds (Sinsch 1991,1992b,2006), and experi-
mental studies in which these cues were manipulated
suggest that the absence of one type of cue can reduce
orientation ability, but no single cue is absolutely essential
for the animals to locate breeding sites (Sinsch 1990a,b).
Available information suggest that magnetic and celestial
cues are primary cues involved in newt’s homing orienta-
tion (Landreth and Ferguson 1967; Phillips 1986,1987;
Phillips and Borland 1994; Phillips et al. 1995; Diego-
Rasilla and Luengo 2002; Diego-Rasilla 2003;Diego-
Rasilla et al. 2005), whereas other orientation cues, such
as odor cues from breeding ponds or acoustic cues, will be
reliable over relatively short distances (Joly and Miaud
1993; Diego-Rasilla and Luengo 2004) and are unlikely to
account for the long-distance homing exhibited by newts,
although these cues might improve accuracy of orientation
during the final approach to the breeding pond and should
increase colonization of ponds near currently used ponds.
The results suggest that it is possible that the individuals
from the lowland population may perform positive phono-
taxis to the sympatric anuran calls because they have
learned to associate these calls with the pond location and,
thus, are able to distinguish the calls from other types of
sound signals. In fact, the population showing the positive
phonotactic response came from a man-made pond less
than 4 years old. However, although this hypothesis is
suggestive, it is not entirely conclusive because it may be
possible that a genetically based recognition system could
also function here, if the frogs and newts co-occur often
enough that the presence of heterospecific signals is part of
the “expected environment.”The advantages of the dem-
onstrated system are clear, so it is theoretically possible that
the distinct behavioral types could arise through selection,
if the newt and frog populations overlapped for a sufficient
1334 Behav Ecol Sociobiol (2007) 61:1329–1335
amount of time. Therefore, although feasible, learning is
not a default conclusion for population differences in
behavior.
Our results confirm that migrating newts can use the
calls of anurans as a guidance mechanism. However, more
research is needed to determine the types of sensory cues
involved in the orientation behavior of L. helveticus, and a
detailed study is now in progress. Furthermore, although
our results support the acoustic orientation hypothesis,
future work should be focused on testing the heterospecific
attraction hypothesis (Mönkkönen et al. 1999). Because the
palmate newts arrived at the garden pond after the Iberian
green frogs, presumably colonizing newts might use the
presence of resident species (Iberian green frogs) as a cue
for profitable aquatic breeding sites. Thus, movements
apparently in response to calls may favor dispersal in newts
(Ferguson and Landreth 1966). Hence, later-arriving indi-
viduals might use the presence of earlier established species
as a cue to profitable breeding sites (i.e., heterospecific
attraction; Mönkkönen et al. 1999).
Acknowledgements We sincerely thank Marcos Diego-Gutiérrez
and Felicidad Rasilla-Fernández for assistance during this study.
Thanks are also due to Richard P. Brown, J. Christensen-Dalsgaard
and two anonymous reviewers for invaluable comments and sugges-
tions regarding the manuscript. The Cantabria autonomous govern-
ment kindly granted the necessary permits for the study. The
experiments reported herein comply with the current laws of Spain.
References
Barbadillo LJ, Lacomba JI, Pérez-Mellado V, Sancho V, López-Jurado
LF (1999) Anfibios y Reptiles de la Península Ibérica, Baleares y
Canarias. Editorial GeoPlaneta, Barcelona
Batschelet E (1981) Circular statistics in biology. Academic, London
Diego-Rasilla FJ (2003) Homing ability and sensitivity to the
geomagnetic field in the alpine newt, Triturus alpestris. Ethol
Ecol Evol 15:251–259
Diego-Rasilla FJ (2004) El sentido magnético y su uso en la
orientación de los animales. In: Pereira D, Bárcena MA, Rubio
I, Sesma J (eds) Aproximación a las Ciencias Planetarias.
Aquilafuente 74. Ediciones Universidad de Salamanca, Sala-
manca, pp 269–297
Diego-Rasilla FJ, Luengo RM (2002) Celestial orientation in the
marbled newt (Triturus marmoratus). J Ethol 20:137–141 DOI
10.1007/s10164-002-0066-7
Diego-Rasilla FJ, Luengo RM (2004) Heterospecific call recognition
and phonotaxis in the orientation behavior of the marbled newt,
Triturus marmoratus. Behav Ecol Sociobiol 55:556–560 DOI
10.1007/s00265-003-0740-y
Diego-Rasilla FJ, Luengo RM, Phillips JB (2005) Magnetic compass
mediates nocturnal homing by the alpine newt, Triturus alpestris.
Behav Ecol Sociobiol 58:361–365 DOI 10.1007/s00265-005-
0951-5
Elmberg J (1990) Long-term survival, length of breeding season, and
operational sex ratio in a boreal population of common frogs,
Rana temporaria L. Can J Zool 68:121–127
Ferguson DE, Landreth HF (1966) Celestial orientation of the fowler’s
toad Bufo fowleri. Behaviour 26:105–123
Fischer JH, Freake MJ, Borland SC, Phillips JB (2001) Evidence for
the use of magnetic map information by an amphibian. Anim
Behav 62:1–10 DOI 10.1006/anbe.2000.1722
Fisher NI (1995) Statistical analysis of circular data. Cambridge
University Press, Cambridge
Hetherington T (2001) Laser vibrometric studies of sound-induced
motion of the body walls and lungs of salamanders and lizards:
implications for lung-based hearing. J Comp Physiol [A]
187:499–507
Joly P, Miaud C (1989) Fidelity to the breeding site in the alpine newt
Triturus alpestris. Behav Processes 19:47–56
Joly P, Miaud C (1993) How does a newt find its pond? The role of
chemical cues in migrating newts (Triturus alpestris). Ethol Ecol
Evol 5:447–455
Landreth HF, Ferguson DE (1967) Newts: sun-compass orientation.
Science 158:1459–1461
Mardia KV, Jupp PE (2000) Directional statistics. Wiley, New York
Márquez R, Mateu E (1995) Sounds of frogs and toads of Spain and
Portugal. ALOSA, sonidos de la naturaleza, Barcelona
Mönkkönen M, Härdling R, Forsman JT, Tuomi J (1999) Evolution of
heterospecific attraction: using other species as cues in habitat
selection. Evol Ecol 13:93–106
Montori A, Herrero P (2004) Lissotriton helveticus (Rauzoumowsky,
1789). In: Ramos MA et al (eds), Amphibia, Lissamphibia. García-
París M, Montori A, Herrero P, Fauna Ibérica, vol 24. Museo
Nacional de Ciencias Naturales, CSIC, Madrid, pp 252–275
Nieto-Román S, Barluenga M, Palanca A, Vences M, Meyer A (2004)
Post-mating clutch piracy in an amphibian. Nature 431:305–308
DOI 10.1038/nature02879
Phillips JB (1986) Two magnetoreception pathways in a migratory
salamander. Science 233:765–767
Phillips JB (1987) Homing orientation in the eastern red-spotted newt
(Notophthalmus viridescens). J Exp Biol 131:215–229
Phillips JB, Borland SC (1994) Use of a specialized magnetoreception
system for homing by the eastern red-spotted newt Notophthal-
mus viridescens. J Exp Biol 188:275–291
Phillips JB, Adler K, Borland SC (1995) True navigation by an
amphibian. Anim Behav 50:855–858
Reques R, Tejedo M (2002) Bufo calamita. In: Pleguezuelos JM,
Márquez R, Lizana M (eds) Atlas y libro rojo de los anfibios y
reptiles de España. Dirección General de Conservación de la
Naturaleza-Asociación Herpetológica Española, Madrid, pp 107–
109
Sinsch U (1990a) The orientation behaviour of three toad species
(genus Bufo) displaced from the breeding site. In: Hanke W (ed)
Fortschritte der Zoologie, vol 38, Biology and physiology of
amphibians. Gustav Fischer Verlag, Stuttgart, pp 73–83
Sinsch U (1990b) Migration and orientation in anuran amphibians.
Ethol Ecol Evol 2:65–79
Sinsch U (1991) The orientation behaviour of amphibians. Herpetol J
1:541–544
Sinsch U (1992a) Sex-biased site fidelity and orientation behaviour in
reproductive natterjack toads (Bufo calamita). Ethol Ecol Evol
4:15–32
Sinsch U (1992b) Amphibians. In: Papi F (ed) Animal homing.
Chapman and Hall, New York, pp 213–233
Sinsch U (2006) Orientation and navigation in Amphibia. Mar Freshw
Behav Physiol 39:65–71
Twitty VC, Grant D, Anderson O (1966) Course and timing of the
homing migration in the newt Taricha rivularis. Proc Natl Acad
Sci USA 56:864–869
Wilczynski W, Ryan MJ (1988) The amphibian auditory system as a
model for neurobiology, behavior, and evolution. In: Fritzsch B,
Ryan MJ, Wilczynski W, Hetherington T, Walkowiak W (eds)
The evolution of the amphibian auditory system. Wiley, New
York, pp 3–12
Behav Ecol Sociobiol (2007) 61:1329–1335
