Introduction

Echolocating bats adapt their echolocation call design to cope with changes in the acoustic environment (Roverud and Grinnell 1985a; Obrist 1995; Neuweiler 2000; Schnitzler and Kalko 2001). In particular, conspecific signals may mask the weak echoes coming from flying insects that are potential prey (Ulanovsky et al. 2004). Several studies have reported that bats modify the spectral–temporal features of their vocalizations to avoid interference with the vocalizations of conspecifics (Habersetzer 1981; Surlykke and Moss 2000; Ibánez et al. 2004; Ratcliffe et al. 2004; Gillam et al. 2007; Bates et al. 2008; Chiu et al. 2009) or even use conspecific-generated acoustic signals to guide orientation (Chiu et al. 2008).

The studies above focused on intraspecifc reactions of bats but jamming avoidance may also occur if different species with similar signal design fly in close vicinity to each other. In contrast to the considerable body of research on intraspecific jamming in bats, the problem of interspecific jamming remains largely unexplored. We addressed the question of interspecific jamming in two species of two European vespertilionid bats, Pipistrellus pipistrellus and Pipistrellus nathusii with similar echolocation calls during search flight. These two Pipistrelle species occur sympatrically across a considerable area in Europe and both species forage over water bodies and in wetlands (Meschede 2004b; Sachteleben et al. 2004). Both species emit signals consisting of frequency modulated (FM) sweeps, starting at 38–70 kHz (P. nathusii) and 50–60 kHz (P. pipistrellus), respectively, and ending with a nearly constant frequency (“CF” or “narrowband”) tail-end. The first harmonic of the narrowband frequency amounts to 36–42 kHz in P. nathusii versus 42–51 kHz in P. pipistrellus. The difference in the narrowband frequency is diagnostic for the two species (Skiba 2003); however, there is overlap in the peak frequencies around 42 kHz (Ahlén and Baagøe 1999).

To avoid jamming, bats typically shift the peak frequency (frequency with maximal energy) of the narrowband component of their echolocation signals (Miller and Degn 1981; Ibánez et al. 2004; Ratcliffe et al. 2004; Ulanovsky et al. 2004). The low frequency CF component appears to be the portion of the call that is most actively protected from interference (Bates et al. 2008) and it can be more reliably recorded in the field than other signal parameters such as highest frequency, call duration or loudness (Lawrence and Simmons 1982; Hartley 1989). Therefore, we concentrated on this call parameter during our study. We tested the hypothesis that the peak frequencies of the narrowband component from samples of bats flying with conspecifics or heterospecifics would vary more than those from samples of bats flying alone. In addition, we predicted that P. pipistrellus, the species with the higher peak frequency of the narrowband component, would shift to higher frequencies if P. nathusii was present, whereas P. nathusii would use lower narrowband frequencies if flying with P. pipistrellus.

Materials and methods

We took sound recordings of P. pipistrellus and P. nathusii from 2006 to 2009 in Upper Bavaria (Germany) at the Inn, Traun and Mangfall rivers and at the lakes Chiemsee and Königsee. In this area the presence of both species was established by the capture of many individuals near the study sites (Meschede 2004b; Sachteleben et al. 2004). Pipistrellus kuhlii, a species which can be very difficult to distinguish from P. nathusii by call analyses, does not occur in this area (Meschede 2004a).

Recordings were made with a Pettersson D1000 Bat Detector which has a built-in high-speed recording system that uses a Compact Flash card as storage medium. The resulting sound files (“wav” format) were transferred to a PC for analysis using a commonly available card reader and analysed using Batsoundpro software (Pettersson). Oscillograms and spectrograms were constructed from 2,048-point fast Fourier transforms (FFT), using a sampling frequency of f = 384 kHz and Hanning window function. The range of peak frequencies of both species overlaps between 41.5 and 42.5 kHz (Skiba 2003). Calls within this range were therefore assigned to P. nathusii or P. pipistrellus only if several other calls within the whole sound file fell within the species-specific ranges below or over the critical section. We analysed files with more than six search phase echolocation signals (without approaches and buzzes) of each species. We recognized sequences in the sound file that contained calls from of two bats based on interpulse intervals, frequency range, and the time course of frequency in consecutive signals. Attribution of sequences to an individual bat was based on similar interpulse intervals among successive calls in call sequences.

Peak frequency was measured in the power spectrum as described by Bartonika et al. (2007). In each sound file we analysed six calls from every individual and calculated the means. We obtained peak frequencies from 392 sound files (=2,352 signals) for the following situations:

  • P. pipistrellus flying alone, i.e., no other bats were present (n = 66)

  • P. pipistrellus flying with P. pipistrellus (n = 61)

  • P. nathusii flying alone (n = 59)

  • P. nathusii flying with P. nathusii (n = 80)

  • P. pipistrellus flying with P. nathusii (n = 63)

  • P. nathusii flying with P. pipistrellus (n = 63).

If P. pipistrellus and P. nathusii were recorded flying together (n = 63), we used these sequences to calculate signal parameters for both species. Similarly, in cases of two conspecifics flying together, signal parameters were calculated from both individuals. We used the Kolmogorov–Smirnov test to determine if the distribution of power spectra differed significantly.

As a consequence of the large sample sizes, we disregarded the effect of Doppler shifts during recording. Doppler shifts may have influenced the overall variability in signals in all recording situations but may not have biased specific species combinations.

Results

In both species the peak frequencies of the narrowband component from samples of bats flying with conspecifics varied more than those from samples of bats flying alone (Figs. 1, 2). The differences in frequency distributions were significant in both species (P. nathusii: Kolmogorov–Smirnov Z = 1.47, p = 0.028; P. pipistrellus: Kolmogorov–Smirnov Z = 2.92, p < 0.001). We observed in P. pipistrellus that bats flying with conspecifics used on average higher frequencies than bats flying alone (44.9 kHz, SD 1.6 versus 46.6 kHz, SD 1.6 Mann–Whitney U test, Z = −5,46, p < 0,001).

Fig. 1
figure 1

Peak frequency histograms of P. pipistrellus flying alone (P.pip. n = 66), with conspecifics (P.pip.–P.pip. n = 61) and with P. nathusii (P.pip.–P.nat. n = 63)

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Fig. 2
figure 2

Peak frequency histograms of P. nathusii flying alone (P.nat. n = 59), with conspecifics (P.nat.–P.nat. n = 80) and with P. pipistrellus (P.nat.–P.pip. n = 63)

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If individuals of the two species were recorded together, we found no change in signal parameters of P. nathusii: The distribution of peak frequencies in P. nathusii flying with P. pipistrellus was very similar to that of P. nathusii flying alone (Fig. 2). In contrast, P. pipistrellus used higher peak frequencies if P. nathusii was present than when flying alone (44.9 kHz, SD 1.6 vs. 45.6 kHz SD 1.2) and the peak frequencies were more evenly distributed (Fig. 1). The difference between samples was significant (Kolmogorov–Smirnov Z = 2.06, p < 0.001).

Discussion

Despite the assumption that jamming avoidance plays a role in many echolocating animals, its relevance for free ranging bats is still unclear. It is possible that the signal-processing abilities of bats are so sophisticated that they need not alter their echolocation signals in many jamming situations (Gillam et al. 2007). Moreover, the importance of jamming avoidance may differ between species depending on call design. As an example, auditory neurons in CF bats using narrowband calls have an extremely narrow-band tuning to the bat’s call frequency (Suga et al. 1987; Neuweiler 2000), making spectral jamming less likely (Jones et al. 1994). European Pipistrelles, however, use calls of a bandwidth, which produces large spectral overlap between both conspecifics and heterospecifics (Skiba 2003). In addition, the foraging activities of both of our study species are often concentrated in habitat that is small in area such as streetlamps, ponds and creeks (Blake et al. 1994; Meschede 2004b; Sachteleben et al. 2004). The effect of limited foraging space in these situations is that several individuals often fly in close vicinity, therefore jamming may be a common issue for foraging bats (Roverud and Grinnell 1985a, b; Ulanovsky et al. 2004). As a consequence, jamming avoidance reactions produced by variation of signal parameters are likely to have evolved.

As predicted, in both species a higher variation of peak frequencies occurred if conspecifics were present. This result can be regarded as an indication of jamming avoidance according to the behaviour found in other bat species (Ibánez et al. 2004; Ratcliffe et al. 2004; Bates et al. 2008). The bats shifted their peak frequency significantly, which enhances differences between individuals. Though the observed shifts occurred within the range of only a few kHz, they are probably suited to reduce the jamming effect. For FM-CF bats using CF-components in the studied frequency range, a psychoacoustic frequency discrimination limen of about 1–2 kHz can be expected (see Stebut and Schmidt 2001). If, e.g., two P. nathusii are calling at 38 and 41 kHz (Fig. 2, most frequently used peak frequencies of bats flying with conspecifics) they should be well able to distinguish their calls.

The degree of jamming avoidance may have been underestimated in this study because we excluded some call sequences between 41.5 and 42.5 kHz as we were unable to assign them to species with any degree of confidence. This process in particular affected the samples of P. pipistrellus flying alone and P. nathusii flying with conspecifics. In both situations peak frequencies tend to fall within the lower (P. pipistrellus) or upper (P. nathusii) species-specific range and the excluded sequences might result in a smaller fraction of calls falling in these ranges in our sample than in nature. Consequently, the response to the presence of conspecifics might be more pronounced than indicated by our data.

Our data indicate that not only intraspecific jamming avoidance, but also interspecific jamming frequently occurs in free ranging bats. As we expected P. pipistrellus reacted not only to other P. pipistrellus but also to P. nathusii flying nearby. They used on average a higher peak frequency, which can be explained by the fact that the FM component of P. nathusii calls overlaps with the narrowband component of P. pipistrellus calls (Fig. 3). Obviously, the FM components of P. nathusii signals are loud enough to have a jamming effect on P. pipistrellus, especially if P. nathusii uses calls with peak frequencies >40 kHz, i.e., at the high-frequency end of its species-specific range where the energy is less concentrated around the peak frequency than in lower frequency calls. High-frequency calls of P. nathusii are therefore well suited to mask P. pipistrellus calls at frequencies below 45 kHz. That P. pipistrellus shifted their frequencies upwards, above the jamming stimulus, could be expected (Gillam et al. 2007) because an upward shift puts the loudest components of the P. nathusii call below the frequency band covered by the P. pipistrellus call. Contrary to our prediction, P. nathusii did not lower the narrowband component of its call if P. pipistrellus was present. One explanation for this pattern is that there are no loud components of P. pipistrellus calls within the range of the narrowband component of P. nathusii (<42 kHz) signals and thus, the jamming effect on P. nathusii is probably only very low.

Fig. 3
figure 3

Spectrogram of the signals of P. pipistrellus and P. nathusii while flying together. Loud parts of the P. nathusii call overlap with the narrowband component of the P. pipistrellus call

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In a similar study, Bartonika et al. (2007) found no indication of jamming avoidance in P. pipistrellus and P. pygmaeus flying together. The peak frequency in P. pygmaeus is typically above 52 kHz, which is clearly above the range of peak frequencies in P. pipistellus which therefore cannot be jammed by P. pygmaeus. However, in contrast to our results in the P. pipistrellus–P. nathusii pairing, the species calling at higher frequency (P. pygmaeus) was not jammed by the lower calling species (P. pipistrellus). Probably the frequency ranges of both species are so far apart, that even high calling P. pipistrellus rarely jam the narrowband component of P. pygmaeus.

Since P. pipistrellus and P. nathusii often forage close together, a regular interspecific jamming of P. pipistrellus by P. nathusii can be assumed to occur. Roverud and Grinnell (1985b) showed that jamming reduces a bat’s ability to discriminate distances thus making the capture of prey more difficult. The use of higher peak frequencies by P. pipistrellus to overcome this problem may result in a reduction of its detection range, because higher frequency signals attenuate more rapidly. However, since P. pipistrellus frequently uses similar peak frequencies if flying alone, the reduction in echolocating ability is probably a minor effect and it remains unknown whether jamming by P. nathusii is of great importance for P. pipistellus in the sense of interspecific competition. In our study areas only small differences in habitat preferences of both species occurred (Zahn et al. 2008). However, we do not have any information on other niche parameters such as the timing of foraging. Therefore, the question of interspecific competition between these species is a potential focus for future research.