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Temperature affects sound production in fish with two sets of sonic organs: The Pictus cat
Journal Pre-proof Temperature affects sound production in fish with two sets of sonic organs: The Pictus cat
Friedrich Ladich, Isabelle Pia Maiditsch PII:
S1095-6433(19)30353-8
DOI:
https://doi.org/10.1016/j.cbpa.2019.110589
Reference:
CBA 110589
To appear in:
Comparative Biochemistry and Physiology, Part A
Received date:
29 August 2019
Revised date:
9 October 2019
Accepted date:
10 October 2019
Please cite this article as: F. Ladich and I.P. Maiditsch, Temperature affects sound production in fish with two sets of sonic organs: The Pictus cat, Comparative Biochemistry and Physiology, Part A(2019), https://doi.org/10.1016/j.cbpa.2019.110589
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© 2019 Published by Elsevier.
Journal Pre-proof
Temperature affects Sound Production in Fish with two Sets of Sonic Organs: the Pictus cat Friedrich Ladich and Isabelle Pia Maiditsch*) Department of Behavioural Biology, University of Vienna Althanstraße 14, 1090 Wien, Austria Corresponding author: [email protected] *) Email: [email protected] Phone: ++ 43 1 4277 45277
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Short title: Temperature affects sounds in catfish
Journal Pre-proof Abstract Sound communication is affected by ambient temperature in ectothermic animals including fishes. The present study examines the effects of temperature on acoustic signaling in a fish species possessing two different sound-generating mechanisms. The Amazonian Pictus catfish Pimelodus pictus produces low-frequency harmonic sounds (swimbladder drumming muscles) and high-frequency stridulation sounds (rubbing pectoral fin spines in the pectoral girdle). Sounds of 15 juveniles were recorded when hand-held after three weeks of acclimation at 30°C, 22°C and again 30°C. The following sound characteristics were investigated: calling activity, sound duration, fundamental frequency of drumming sounds and
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dominant frequency of stridulation sounds. The number of both sound types produced within
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the first minute of experiments did not change with temperature. In contrast, sound duration was significantly shorter at 30°C than at 22°C (drumming: 78-560 ms; stridulation: 23-96
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ms). The fundamental frequency of drumming sounds and thus the drumming muscle
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contraction rate varied from 127 Hz to 242 Hz and increased with temperature. The dominant frequency of broadband stridulation sounds ranged from 1.67 kHz to 3.39 kHz and was
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unaffected by temperature changes. Our data demonstrate that temperature affects acoustic signaling in P. pictus, although the changes differed between sound characteristics and sound
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type. The effects vary from no change in calling activity and dominant frequency, to an increase in fundamental frequency and shortened duration of both sound types. Together with
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the known effects of temperature on hearing in the Pictus cat, the present results indicate that
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global warming may affect acoustic communication in fishes.
Keywords: drumming sound, stridulation sound, calling activity, call length, fundamental frequency, dominant frequency, acoustic communication, global warming, temperature
Journal Pre-proof Introduction Temperature plays a role when ectothermic animals such as insects, fish and amphibians communicate acoustically. Temperature effects are known on hindbrain central pattern generators controlling the activity of sonic muscles as well as on sensory organs and behaviour (Brenowitz et al., 1985; Bass and Baker, 1991; Gerhardt and Huber, 2002; Bass et al., 2015; Ladich, 2018). Fishes have probably evolved the largest diversity of sound-generating mechanisms (sonic organs) among vertebrates. According to the morphological structures involved, sonic organs may be classified into swim bladder, pectoral and head mechanisms (Ladich and
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Winkler, 2017). Swim bladder mechanisms are the most common and are based on fast-
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contracting muscles termed drumming (or vocal, or sonic) muscles that vibrate the swim bladder rapidly (Ladich and Bass, 2011; Ladich, 2014). Typically, one muscle contraction
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produces one sound pulse in single contraction calls, and the number of muscle contractions
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per second (muscle contraction rate) equals the fundamental frequency of long duration tonal drumming sounds composed of multiple contractions. The swim bladder muscles may be
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subdivided into intrinsic and extrinsic types, which refers to the fact that the drumming muscles are either entirely attached to the swim bladder or originate on additional structures
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such as bones (Ladich and Fine, 2006). The following sentence needs improving: Despite the many descriptions of sound-producing mechanisms, it is unknown how many of the 30,000+
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extant fish species emit acoustic signals for communication (Nelson et al., 2016). Cartilaginous species and many bony fishes lack sonic organs and are not known to
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communicate acoustically. Surprisingly, even closely related species such as representatives of Scorpaenidae (rockfishes) or Serrasalmidae (piranhas) evolved a diversity of mechanisms or may not be vocal (Hallacher, 1974; Melotte et al., 2019). Some fish species even possess two sound-generating mechanisms, enabling them to produce sounds covering different frequency ranges, typically a low-frequency and a highfrequency sound type. Representatives of several catfish families such as pimelodids, doradids, ariids and mochokids evolved various drumming muscles vibrating the swimbladder and a pectoral stridulatory mechanism (Fine and Ladich, 2003; Ladich and Bass, 2011; Ladich and Fine, 2006). The former muscles result in the emission of low-frequency drumming sounds with main energy below 500 Hz (Ladich et al., 1997). The latter mechanisms consist of enhanced first pectoral fin rays, termed pectoral spines, whose basal, ridged process rubs in a groove of the shoulder girdle and produces series of broadband pulses with main energy extending up to several kilohertz (Ladich, 1997; Papes and Ladich, 2011). Seahorses represent
Journal Pre-proof a second group of fishes emitting low-frequency drumming sounds (generated by an unknown mechanism) and high-frequency click sounds generated by rubbing two occipital bones (Colson et al., 1998; Oliveira et al., 2014). Temperature can affect sound production in fishes in several ways. First, it may change the calling activity, namely the number of sounds emitted in a certain time period. To study the effects of temperature on calling activity in the field is challenging. Additional ecological factors such as season, daily and lunar rhythms or water depth may influence calling (reviewed by Ladich, 2018). Under controlled laboratory conditions, contrasting results have been reported: no dependency of calling activity on temperature (juvenile grey
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gurnards Eutrigla gurnardus, Triglidae) versus an increase with temperature (juvenile Jarbua
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terapon Terapon jarbua, Terapontidae) (Schneider, 1964; Amorim, 2005). This is mirrored in field studies on the oyster toadfish Opsanus tau (Batrachoididae), some of which showed an
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increase of sound production with temperature, others no such effect (Fine, 1978; Montie et
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al., 2015, Ricci et al., 2017, Van Wert et al., 2019). This demonstrates that additional ecological constraints influenced calling activity.
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Beyond affecting calling activity, ambient temperature may influence the temporal and spectral characteristics of acoustic signals. The former includes sound duration, pulse periods,
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pulse repetition rates, fundamental or dominant frequencies of sounds, and perhaps sound levels. Those sound properties that directly depend on fast muscle contractions will be more
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affected by temperature than others. This is particularly the case in swim bladder drumming sounds generated by fast contractions of drumming muscles (Fine, 1978; Ladich, 1997;
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Connaughton et al., 2000; Amorim et al., 2006). The situation is very similar in gobies (Gobiidae), even though sounds are produced by a pectoral sonic muscle (Torricelli et al., 1990; Vincente et al., 2015; Parmentier et al., 2013, 2017). Generally, the drumming muscle contraction rate (pulse repetition rate, fundamental frequency) of drumming sounds increases with temperature. The situation is more complex in species emitting broadband pectoral sounds. Pulse periods may decrease when temperature increases, such as in the croaking gourami Trichopsis vittata (Ladich and Schleinzer, 2015). Elsewhere, no clear effects of temperature of the stridulatory sounds were reported, e.g. in the Striped raphael catfish Platydoras armatulus (Papes and Ladich, 2011). Mohajer et al. (2015) hypothesized that the frequencies of stridulatory sounds are primarily determined by inherent properties of the pectoral girdle in the blue catfish Ictalurus furcatus The present study is designed to investigate the effects of temperature on (1) calling activity and (2) temporal and spectral characteristics of sounds as well as (3) to address the
Journal Pre-proof question to which degree temperature differently affects sounds produced by two sonic mechanisms. A representative of the Amazonian catfish family Pimelodidae was chosen because it readily emits both types of sounds under hand-held conditions. Together with the known effects of temperature on hearing in P. pictus (Wysocki et al., 2009), the results shed some light on the potential influence on global warming on sound communication in fishes. Methods Animals Fifteen juvenile Pictus cats Pimelodus pictus (Pimelodidae) were investigated during this study (see Table 1 for size of fish). Sexing was not possible without killing the animals. They
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were kept in a community tank (100 x 50 x 50 cm) equipped with a layer of sand, roots,
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flower pots and plants as hiding places in a 12-h light – 12 h dark cycle. Fish were fed chironomid larvae except on recording days. The water temperature was controlled by
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submersible heaters and a water cooler (Hailea HC-250A) connected to an external filter.
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Sound Recording
The temperature in the community tank was increased or decreased by 1°C per day until the
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final temperatures were achieved. Fish were acclimated to these experimental temperatures for at least 3 weeks, first to 30°C, then to 22°C and finally again to 30°C.
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Sound recordings were conducted in a round plastic tub (35 cm diameter, 15 cm height, lined on the inside by acoustically absorbent material and a layer of fine sand). The
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water temperature was either 30 ± 1°C or 22 ± 1°C. Catfish were hand-held at a distance of 3 to 5 cm from the hydrophone, which was positioned in the middle of the recording tank. In
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order to avoid overlap of stridulation sounds generated simultaneously by both pectoral fins, one fin was fixed with a finger.
Sounds were recorded using a hydrophone (Brüel & Kjaer 8101) connected to a microphone power supply (Brüel & Kjaer 2408) which was connected to an external sound card (Edirol UA 25EX) of a laptop (Getac 300 B). The laptop ran Cool Edit 2000 (Syntrillium Software Corporation, Phoenix, AZ), and sounds were recorded at a sampling rate of 44.1 or 32 kHz. Sound Analysis Sounds were analyzed using Cool Edit 2000 and STX Sound Tools 3.7.8 developed by the Institute of Sound Research (Austrian Academy of Sciences, Vienna). All sound recordings were low pass filtered (5 kHz) to eliminate resonant frequencies using Cool Edit 2000. The following sound characteristics were determined in drumming and stridulation sounds. The calling activity represents the number of drumming or stridulation sounds
Journal Pre-proof produced within the first minute of sound recording, starting with the onset of the first sound. Duration of drumming and stridulatory sounds (ms) is the time between the onset of the first pulse until the end of the last. Fundamental frequency of drumming sounds (Hz) represents the frequency of lowest (1st ) harmonic. Dominant frequency (kHz) of stridulation sounds is the frequency with the highest amplitude (Fig. 1). Frequencies were measured using power spectra generated in STX (filter bandwidth 10 Hz, overlap 75 %, hanning filter).
Statistics Sound characteristic of 1 to 15 sounds per signal type were measured per specimen and the
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means calculated. These means were then used for further statistics. All data were tested for
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normal distribution using the Shapiro-Wilk test. When data were normally distributed, parametric statistical tests were applied, in other cases non-parametric tests were used.
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Because fish could be individually recognized based on the patterns of their spots, a repeated
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measures (RM) general linear model (GLM, ANOVA) was calculated followed by a Bonferroni post hoc test. If data were not normally distributed, a Friedman test was followed
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by a Dunn-Bonferroni post hoc test to reveal differences between temperatures. All statistical tests were run using IBM SPSS Statistics Version 26.
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Ethical considerations
All applicable national and institutional guidelines for the care and use of animals were
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followed (permit number BMWFW-66.006/0035-WF/V/3b/2017 by the Austrian Federal
Results
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Ministry of Science, Research and Economy).
Drumming and stridulation sounds Pictus cats produced drumming and stridulation sounds either separately from each other or at the same time. The drumming sound consisted of a series of low-frequency pulses with a rather constant pulse period, yielding harmonic sounds. The main energy of drumming sounds was concentrated in the fundamental frequency (1st harmonic) at approximately 120 to 200 Hz or in the second harmonic (Fig. 1, Fig. 2a, b). The drumming sound may consist of (a) a series of pulses of very similar amplitude, resulting in a long continuous drumming sound (Fig. 2a) or of (b) a series of short drumming sounds (bursts) or (c) of various intermediate stages. Figure 2b shows a series of 11 short drumming sounds of which the fourth, fifth and sixth merge into one another. Stridulation sounds are produced during abduction of pectoral spines in Pictus cats. In contrast to drumming sounds, they were built up of a series of short broadband pulses with
Journal Pre-proof main energies concentrated between 1 and 3 kHz (Fig. 3). Thus, main energies were clearly higher than in drumming sounds (Fig. 1, 4). The intervals between pulses were not as regular as in drumming sounds but varied considerably. Rather, they were typically large in the middle part of the sounds and small toward the beginning and end of the sounds (Figs. 3, 4). Size and calling activity Fish weight changed significantly over the course of experiments (RM-GLM: F2, 28 = 45.76, p < 0.001). Bonferroni post hoc tests revealed that fish gained weight between the first and second measurement but not between the second and third (Table 1). Nonetheless, changes in sound characteristics were independent of changes in body weight.
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The number of sounds produced by specimens within the first minute of sound
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recording ranged from no sounds to 71 in drumming sounds and from no sounds to 60 in stridulation sounds. The calling activity did not change with temperature either in drumming
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sounds (Friedman’s test: Chi-Square = 0.964, N = 15, df = 2, n.s.) or in stridulation sounds
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(Friedman’s test: Chi-Square = 5.193, N = 15, df = 2, n.s.) (Table 1). Temporal sound characteristics
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Both sound types of Pictus cats were longer at the lower temperature. The mean length of drumming sounds of specimen over all experiments ranged from 77.7 ms to 560 ms and
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increased significantly at 22°C (RM-GLM: F2, 24 = 16.56, p < 0.001) (Fig. 5a). Bonferroni post hoc tests revealed no difference between the 30°C measurements.
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Stridulation sounds were also shorter at 30°C than at 22°C (RM-GLM: F2, 18 = 29.28,
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p < 0.001) (Fig. 5a). The mean individual duration ranged from 23 ms to 103 ms over all experiments. Bonferroni post hoc tests revealed no difference between sounds produced at the 30°C measurements. Stridulation sounds were shorter than drumming sounds at all temperatures (Paired-samples T-test: 30°C: t = 6.94, df = 12, p < 0.001; 22°C: t = 12.80, df = 12, p < 0.001; 30°C repeated: t = 6.04, df = 12, p < 0.001) (Table 1). Table 1. Mean (± S.E.) body weight, calling activity (number of sounds) and sound characteristics of drumming (DR) and stridulation sounds (SR) of Pictus cats at the experimental temperatures. The range is given in brackets. The second number in brackets gives the number of sound-producing individuals.
Variable
Body weight (g)
30°C
22°C
30°C
3.61 ± 0.14
4.54 ± 0.14
4.80 ± 0.22
(2.5 - 4.5)
(3.5 - 5.6)
(3.43 - 6.12)
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Sound duration DR (ms)
Sound duration SR (ms)
Fundamental frequency DR (Hz)
10.20 ± 1.82
9.27 ± 1.76
(1 - 71; 15)
(0 - 28; 14)
(0 - 24; 14)
9.40 ± 2.74
17.67 ± 3.24
12.0 ± 3.84
(0 - 34; 13)
(0 - 40; 13)
(0 - 60; 13)
241.6 ± 25.1
437.1 ± 23.3
273.8 ± 37.9
(77.7 - 408.5)
(231.9 - 600.1)
(109.2 - 559.6)
39.49 ± 3.44
83.17 ± 3.59
39.41 ± 3.32
(23.0 - 68.0)
(61.9 - 103)
(19.3 - 64.9)
220.2 ± 3.60
142.7 ± 2.53
212.8 ± 2.46
(190.6 - 242.2)
(126.7 - 156.3)
(186.2 - 225.0)
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Sound number SR
14.53 ± 4.66
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Sound number DR
2.512 ± 134 Dominant frequency SR (kHz)
2.274 ± 100
2.154 - 2.793)
(1.666 - 2.957)
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(1.912 - 3.391)
2.508 ± 51
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Spectral characteristics of sounds
The fundamental frequency of drumming sounds differed significantly with temperature
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(Friedman’s test: Chi-Square = 20.46, N = 13, df = 2, p < 0.001). The mean fundamental frequency ranged from 127 Hz to 242 Hz. Dunn-Bonferroni post hoc tests revealed that the
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fundamental frequency is lower at 22°C than at both 30°C measurements (Fig. 6a). The dominant frequency of stridulation sounds also differed between experiments
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(RM-GLM: F2, 18 = 6.663, p < 0.007), with mean individual frequencies ranging from 1.67
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kHz to 3.40 kHz. Bonferroni post hoc tests revealed no difference between the sounds recorded in the first experiment at 30°C and those recorded at 22°C on the second trial. There was a difference between sounds emitted at 22°C and those produced on the third attempt at 30°C (Fig. 6b). Thus, there is no clear temperature effect on the dominant frequencies of stridulation sounds. Discussion Sound production during hand-held conditions has been frequently described in fishes (e.g. Salmon, 1967; Ladich, 1997; Heyd and Pfeiffer, 2000; Melotte et al., 2016). The emission of sounds in distress situations including sounds uttered when predators approach or even grab prey fish raises the question on its functional significance. So far no evidence is available to suggest that such fish try to warn conspecifics or successfully deter predators (Markl, 1968; Myrberg, 1981;, Bosher et al., 2006; Bessey and Heithaus, 2013). Our current lack of information, however, does not exclude that sound production under these conditions is a means of intra- or interspecific acoustic communication.
Journal Pre-proof Calling activity The number of sounds (drumming and stridulation sounds) produced by Pictus cats did not depend on temperature in the present study. Numerous field and lab studies have investigated the effects of temperature on fish vocalizing activity (Ladich, 2018). Despite the wide variety of experimental setups and species chosen, no clear temperature effect on calling activity was found. Laboratory studies can control various parameters such as the light cycle, making it easier to describe solely the influence of temperature on sound production. In the lab, for example, an increase in calling activity with temperature was described in the gudgeon Gobio gobio (Cyprinidae), the Jarbua terapon Terapon jarbua (Terapontidae),
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the bullhead Cottus gobio (Cottidae) and the red drum Sciaenops ocellatus (Sciaenidae)
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during seasonal light regimes or 12h:12h light cycles (Schneider, 1964; Ladich, 1988; 1989, Montie et al., 2016). In contrast, no such temperature effects were observed in the painted
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goby Pomatoschistus pictus (Gobiidae), the grey gurnard Eutrigla gurnardus (Triglidae) and
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the Atlantic cod Gadus morhua (Gadidae) (Brawn, 1961; Amorim, 2005; Vicente et al., 2015).
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In field studies as well, both an increase in calling activity with temperature and no effect have been reported even in the same species. This is less of a surprise considering the
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large number of factors involved besides temperature. For example, the number of individuals calling on different recording days remains unknown. In the frequently investigated oyster
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toadfish, conflicting results are reported. Montie et al. (2015) noted an increase in the number of boatwhistles — the advertising calls of the oyster toadfish — in the May River, South
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Carolina, whereas no such correlations to temperature were described by others, although seasonal, lunar and daily calling rhythms were distinguished (Monczak et al., 2017; Ricci et al., 2017). Amorim et al. (2006) observed a seasonal increase in calling activity with temperature
in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae) in the Tagus estuary, Portugal, and a drop in sound production in late July at high temperatures. Furthermore, water depth may affect calling. A seasonal increase in sound production was reported in the spotted weakfish Cynoscion nebulosus (Sciaenidae), particularly in deeper water (Montie et al. 2015). In summary, calling activity apparently increases with temperature in most species, parallel to a general increase in agonistic and reproductive behaviour. The lack of a temperature effect in this parameter, such as in the Pictus cat, may have numerous reasons. One might be the behavioural context: distress situations, for example, are not necessarily related to reproductive behaviour. Another potential explanation is that distress levels vary considerably between individuals, which could mask a significant difference between
Journal Pre-proof temperatures. In the Pictus cat, the number of drumming sounds emitted within the first minute on the first recording day varied from 1 to 71 between individuals. Similarly, Fine and Waybright (2015) reported that the number of grunts in a train and other sound properties were highly variable in oyster toadfish when specimens were recorded twice. Temporal characteristics The duration of both sound types was clearly temperature-dependent in the Pictus cat. Drumming and stridulation sounds were about half as long at 30°C as at 22°C. This can be explained by higher firing rates of central pattern generators und subsequently faster contractions of muscles at the higher temperature (Bass et al., 2015). A similar observation
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was made for the pectoral sounds in Platydoras armatulus and Trichopsis vittata (Ladich and
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Schleinzer, 2015). In P. armatulus, stridulation sounds emitted both during abduction and adduction of the large pectoral spines were shorter at 30°C than at 22°C (Papes and Ladich,
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2011)
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The duration of drumming sounds was clearly temperature-dependent in Pictus cats, but no such effect was observed in other species such as in P. armatulus sounds recorded in
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the same behavioural context or in the mating calls of the oyster toadfish (Fine, 1978; Papes and Ladich, 2011). The shorter total duration in the Pictus cat may partly be explained by
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faster muscle contraction – as long as the number of muscle contractions is similar at all temperatures (as is the case in stridulation sounds, where the number of pulses is largely
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limited by the number of ridges on the proximal end of the pectoral spine) (Fine and Ladich 2003). However, the number of muscle contractions and thus pulses is not limited in
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drumming sounds, helping to explain why potential temperature effects on sound length may be missing (Fine, 1978). There is evidence that separate pattern generators in the hindbrain code the pulse repetition rate (fundamental frequency) and call duration in fishes (Bass et al., 2015). Vocal pacemaker nuclei (VPN) determine the pulse repetition rate, whereas vocal prepacemaker (VPP) neurons determine the duration of calls. The effect of temperature on sound duration is even more complex. In the Pictus cat, drumming and stridulation sounds became shorter at 30°C even though they are being produced by different sonic mechanisms in the same (distress) context. In contrast, opposite effects may be observed in different behavioural contexts in sounds produced by the same sonic organs within a species. Amorim et al. (2006) described an increase in the duration of boatwhistles, the mating signal of the toadfish H. didactylus, which are produced by their intrinsic swimbladder muscles. At the same time, Amorim et al. (2006) observed a decrease in the duration of croaks, an agonistic call.
Journal Pre-proof Spectral characteristics of sounds The fundamental frequency of drumming sounds in Pictus cats increased significantly with ambient temperature. The fundamental frequency or pulse repetition rate of drumming sounds is the sound property most regularly affected by temperature. This effect has been demonstrated in nearly all studies investigating temperature effects on sound production in fishes such as toadfishes, piranhas, searobins, gobies, drums, etc. (Fine, 1978; Kastberger 1981; Brantley and Bas,s 1994; Lugli et al., 1996; Connaughton, 2004; Connaughton et al., 2002; Maruska and Mensinger, 2009, Ladich, 2018). The increase in fundamental frequency demonstrates the importance of temperature on the firing rate of central pattern generators and
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on sonic muscle contraction rates.
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In contrast, the dominant frequency of pectoral stridulation sounds shows no clear difference between temperatures, similarly to the fundamental frequency, and seems to be
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independent of temperature. This can partly be explained by the difficulty in measuring the
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dominant frequency of a stridulation sound. The sound energy is broadly distributed within a stridulation sound, and main energies may in addition switch in frequency range between
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adjacent pulses within a stridulation sound (see sonagrams). This complicates determining the frequency with the highest amplitude. Accordingly, the mean dominant frequency varied
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considerably between individual fish within one measurement, ranging from 1912 Hz to 3174 Hz at the first 30°C measurement.
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A lack of a temperature dependency of dominant frequencies was also observed in a prior study on doradid stridulation sounds. In P. armatulus, Papes and Ladich (2011)
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described differences in the dominant frequency when shifting from 22°C to 30°C but not from 30°C to 22°C when the lower temperature experiments were repeated. In contrast, the dominant frequency of croaking sounds in the gourami T. vittata was affected by temperature. Ladich and Schleinzer (2015) observed an increase from 1221 Hz at 25°C to 1270 Hz at 30°C to 1341 Hz at 35°C. The dominant frequency was lower at the first two temperatures as compared to the highest one. These differences between catfishes and croaking gourami most likely reflect their different sound-generating mechanisms. Trichopsis vittata produces pectoral sounds by plucking enhanced tendons in its pectoral fins, whereas catfishes rub their pectoral spines in the pectoral girdle (Fine and Ladich, 2003; Ladich and Fine, 2006). The dominant frequency of croaking sounds in T. vittata seems to be based on to the speed of pectoral muscle contractions and on the resonances of their air-breathing cavity (suprabranchial air-breathing organ) adjacent to the pectoral girdle. In catfishes the frequency spectrum appears to be determined primarily by the pectoral girdle, not by the swimbladder.
Journal Pre-proof Fine et al. (1997) removed the air in the swimbladder of the channel catfish Ictalurus punctatus and found that the frequency spectra were similar before and after deflation, indicating that the swimbladder plays no major role in determining the sound frequency. Mohajer et al. (2015) demonstrated that different pectoral fin speeds resulted in a rather similar frequency spectrum, indicating that the spectrum is dictated primarily by the natural frequency of the pectoral girdle. Thus, a strong temperature effect on pectoral sounds cannot be expected. Did significant changes in fish size during the course of the experiments effect sound characteristics in the Pictus cat? None of the determined sound properties changed in parallel
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with body weight. Neither the lack of a change in calling activity, the decrease in call lengths
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nor the increase in fundamental frequency were paralleled by changes in body size. Conclusion
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The current study reveals that ambient temperature does not affect acoustic signals produced
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by fundamentally different sonic mechanisms in the same ways within one species. The number of drumming and stridulation sounds produced by the Pictus cat does not depend on
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temperature. This may be explained by the fact that both sounds were emitted in the same behavioural context and that the fish may be similarly stressed at both temperatures. The
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shorter duration of both sound types at the higher temperature is due to the central pattern generators and thus higher speed of swimbladder and pectoral muscle contractions at 30°C.
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Finally, we attribute the differences in temperature dependency of the spectral characteristics of sounds (fundamental and dominant frequency) to the fundamental difference in sound-
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generating mechanisms.
Despite differences in the properties of low- and high-frequency sounds, ambient temperature clearly affected acoustic signaling in the Pictus cat. This is paralleled by temperature-dependent differences in hearing (Wysocki et al., 2009). The Pictus cat is more sensitive at higher temperatures. We currently know next to nothing about whether the changes in sound characteristics are coupled to temperature-dependent changes in hearing sensitivities in fishes, as is the case in frogs (Gerhardt, 1978). One study in the midshipman Porichthys notatus indicates that such a phenomenon exists in fishes (McKibben and Bass, 1998). The temperature dependency of acoustic signaling and hearing sensitivity, and of the potential coupling between both, raises the question whether global warming affects sound communication in fishes. Narins and Meenderink (2014) predict that ongoing temperature change will effectively uncouple the sound production and detection systems in frogs,
Journal Pre-proof affecting acoustic communication negatively. We expect similar developments in vocal fish taxa. Acknowledgements We thank Min Chai, Joana Schär and Sandra Weber for their help in collecting data, Michael Stachowitsch for scientific English proofreading and two reviewers for helpful comments. This study was supported by the Austrian Science Fund (FWF grant no. P31045). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Conflict of Interests The authors declare no conflict of interest. Supplementary material
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S1: Recording of a long drumming sound of a Pictus cat illustrated in figure 2a. S2: Recording of a series of 11 short drumming sounds illustrated in figure 2b.
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S3: Recording of three stridulation sounds illustrated in figure 3. S4: Recording of a drumming and stridulation sound emitted simultaneously and illustrated in
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figure 4. References
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Amorim, M. C. P. and Hawkins, A. D. (2005). Ontogeny of acoustic and feeding behaviour in
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in vertebrates. In Communication in Fishes: 3-43. Ladich, F., Collin, S. P., Moller, P. and Kapoor, B. G. (Eds.). Enfield, NH: Science Publishers. Ladich, F. and Bass, A. H. (2011). Vocal Behavior of Fishes: Anatomy and Physiology. In Encyclopedia of Fish Physiology: From Genome to Environment: 321-329. Farrell, A. P. (Ed.) San Diego: Academic Press. Ladich, F. and Schleinzer, G. (2015). Effect of temperature on acoustic communication: Sound production in the croaking gourami (labyrinth fishes). Comparative Biochemistry and Physiology, Part A 182: 8-13. Ladich, F. and Winkler, H. (2017). Acoustic communication in terrestrial and aquatic vertebrates. Journal of Experimental Biology 220: 2306-2317. Lugli, M., Torricelli, P., Pavan, G. and Miller, P. J. (1996). Breeding sounds of male Padogobius nigricans with suggestions for further evolutionary study of vocal behaviour in gobioid fishes. Journal of Fish Biology 49: 648-657.
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Mélotte, G., Raick, X., Vigouroux, R. and Parmentier, E. (2019). Origin and evolution of
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catfish Ictalurus furcatus. Journal of Comparative Physiology A 201: 305-315.
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Monczak, A., Berry, A., Kehrer, C. and Montie, E. W. (2017). Long-term acoustic monitoring of fish calling provides baseline estimates of reproductive timelines in the May River estuary,
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southeastern USA. Marine Ecology Progress Series 581: 1-19. Montie, E. W., Vega, S. and Powell, M. (2015). Seasonal and spatial patterns of fish sound
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Montie, E. W., Kehrer, C., Yost, J., Brenkert, K., O’Donnell, T. and Denson, M. R. (2016). Long-term monitoring of captive red drum Sciaenops ocellatus reveals that calling incidence
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and structure correlate with egg deposition. Journal of Fish Biology 88: 1776-1795. Myrberg, A. A. (1981). Sound communication and interception in fishes. In Hearing and Sound Communication in Fishes: 395-426. Tavolga, W. N., Popper, A. N. and Fay, R. R. (Eds.). New York: Springer.
Narins, P. M. and Meenderink, S. W. F. (2014). Climate change and frog calls: long-term correlations along a tropical altitudinal gradient. Proceedings of the Royal Society B, Biological Sciences 281: 20140401. Nelson, J. S., Grande, T. C. and Wilson, M. V. H. (2016). Fishes of the World. (5 edn). Hoboken, New Jersey: John Wiley & Sons, Inc. Oliveira, T. P. R., Ladich, F., Abed-Navandi, D., Souto, A. S. and Rosa, I. L. (2014). Sounds produced by the longsnout seahorse: a study of their structure and functions. Journal of Zoology 294: 114-121.
Journal Pre-proof Papes, S. and Ladich, F. (2011). Effects of temperature on sound production and auditory abilities in the Striped Raphael Catfish Platydoras armatulus (Family Doradidae). PLoS ONE 6: e26479. Parmentier, E., Kéver, L., Boyle, K., Corbisier, Y.-E., Sawelew, L. and Malavasi, S. (2013). Sound production mechanism in Gobius paganellus (Gobiidae). The Journal of Experimental Biology 216: 3189-3199. Parmentier, E., Petrinisec, M., Fonseca, P. J. and Amorim, M. C. P. (2017). Sound-production mechanism in Pomatoschistus pictus. Journal of Experimental Biology 220: 4374-4376. Ricci, S. W., Bohnenstiehl, D. R., Eggleston, D. B., Kellogg, M. L. and Lyon, R. P. (2017).
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oyster restoration site. PLOS ONE 12(8): e0182757.
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Oyster toadfish (Opsanus tau) boatwhistle call detection and patterns within a large-scale
Salmon, M. (1967). Acoustic behavior of the Menpachi, Myripristis berndti, in Hawaii.
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Pacific Science 11: 364-381.
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Schneider, H. (1964). Physiologische und morphologische Untersuchungen zur Bioakustik der Tigerfische (Pisces, Theraponidae). Zeitschrift für vergleiche nde Physiologie 47: 493-558.
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Torricelli, P., Lugli, M. and Pavan, G. (1990). Analysis of sounds produced by male Padogobius martensi (Pisces: Gobiidae) and factors affecting their structural properties.
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Bioacoustics 2(4): 261-276.
Van Wert, J. C. and Mensinger, A. F. (2019). Seasonal and daily patterns of the mating calls
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of the oyster toadfish, Opsanus tau. The Biological Bulletin: doi: 10.1086/701754. Vicente, J. R., Fonseca, P. J. and Amorim, M. C. P. (2015). Effects of temperature on sound
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production in the painted goby Pomatoschistus pictus. Journal of Experimental Marine Biology and Ecology 473: 1-6.
Wysocki, L. E., Montey, K. and Popper, A. N. (2009). The influence of ambient temperature and thermal acclimation on hearing in a eurythermal and a stenothermal otophysan fish. Journal of Experimental Biology 212: 3091-3099. Figure legends Fig. 1. Sound spectrum of a drumming- and a stridulation sound emitted simultaneously (see also Fig. 4) by a Pictus cat showing the difference in energy content of both sound types and frequencies measured. The fundamental frequency (FF) was determined in drumming sounds and the dominant frequency (DF) in stridulation sounds. Note the harmonic content of the drumming sound with the fundamental frequency and the second harmonic (asterisk) containing the highest energy. Sampling frequency 44.1 kHz, filter bandwidth 10 Hz, overlap 75%, hanning window.
Journal Pre-proof Fig. 2. Sonagram and oscillogram of (a) a long, continuous drumming sound and (b) a drumming sound consisting of a series of 11 short drumming sounds (bursts) emitted by a Pictus cat. Note in (b) that short bursts 4, 5 and 6 are not clearly separated. Sampling frequency 44.1 kHz, filter bandwidth 25 Hz, overlap 75%, hanning window. Fig. 3. Sonagram and oscillogram of three stridulation sounds emitted independently from drumming sounds by a Pictus cat. Note that the main sound energies are located between 1 and 3 kHz. Sampling frequency: 32 kHz, filter bandwidth 225 Hz, overlap 75%, Hanning filter. Fig. 4. Sonagram and oscillogram of a drumming sound and a stridulation sound produced
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simultaneously by a Pictus cat, illustrating the difference in sound length and frequency
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content. Note that the difference in drumming sounds shown in Fig. 2 and Fig. 4 is due to different filter bandwidth. Sampling frequency 44.1 kHz, filter bandwidth 250 Hz, overlap
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75%, hanning window.
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Fig. 5. Mean (+ S.E.) (a) duration of drumming sounds at different temperatures and of (b) stridulation sounds at different temperatures. Different letters above bars indicate significant
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differences between temperatures (P < 0.05).
Fig. 6. Mean (+ S.E.) (a) fundamental frequency of drumming sounds at different
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temperatures and (b) dominant frequency of stridulation sounds at different temperatures.
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Graphical abstract
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Different letters above bars indicate significant differences between temperatures (P < 0.05).
Journal Pre-proof Highlights (Bullet points) Acoustic signaling in fishes is variously influenced by ambient temperature. Pictus catfish emit low-frequency drumming and high- frequency stridulation sounds. Number of emitted drumming and stridulation sounds did not change with temperature. Temporal sound characteristics were similarly, spectral properties differently affected. Temperature effects depend on sound characteristic and sonic mechanism in Pictus
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cats.
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Friedrich Ladich, Isabelle Pia Maiditsch PII:
S1095-6433(19)30353-8
DOI:
https://doi.org/10.1016/j.cbpa.2019.110589
Reference:
CBA 110589
To appear in:
Comparative Biochemistry and Physiology, Part A
Received date:
29 August 2019
Revised date:
9 October 2019
Accepted date:
10 October 2019
Please cite this article as: F. Ladich and I.P. Maiditsch, Temperature affects sound production in fish with two sets of sonic organs: The Pictus cat, Comparative Biochemistry and Physiology, Part A(2019), https://doi.org/10.1016/j.cbpa.2019.110589
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© 2019 Published by Elsevier.
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Temperature affects Sound Production in Fish with two Sets of Sonic Organs: the Pictus cat Friedrich Ladich and Isabelle Pia Maiditsch*) Department of Behavioural Biology, University of Vienna Althanstraße 14, 1090 Wien, Austria Corresponding author: [email protected] *) Email: [email protected] Phone: ++ 43 1 4277 45277
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Short title: Temperature affects sounds in catfish
Journal Pre-proof Abstract Sound communication is affected by ambient temperature in ectothermic animals including fishes. The present study examines the effects of temperature on acoustic signaling in a fish species possessing two different sound-generating mechanisms. The Amazonian Pictus catfish Pimelodus pictus produces low-frequency harmonic sounds (swimbladder drumming muscles) and high-frequency stridulation sounds (rubbing pectoral fin spines in the pectoral girdle). Sounds of 15 juveniles were recorded when hand-held after three weeks of acclimation at 30°C, 22°C and again 30°C. The following sound characteristics were investigated: calling activity, sound duration, fundamental frequency of drumming sounds and
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dominant frequency of stridulation sounds. The number of both sound types produced within
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the first minute of experiments did not change with temperature. In contrast, sound duration was significantly shorter at 30°C than at 22°C (drumming: 78-560 ms; stridulation: 23-96
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ms). The fundamental frequency of drumming sounds and thus the drumming muscle
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contraction rate varied from 127 Hz to 242 Hz and increased with temperature. The dominant frequency of broadband stridulation sounds ranged from 1.67 kHz to 3.39 kHz and was
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unaffected by temperature changes. Our data demonstrate that temperature affects acoustic signaling in P. pictus, although the changes differed between sound characteristics and sound
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type. The effects vary from no change in calling activity and dominant frequency, to an increase in fundamental frequency and shortened duration of both sound types. Together with
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the known effects of temperature on hearing in the Pictus cat, the present results indicate that
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global warming may affect acoustic communication in fishes.
Keywords: drumming sound, stridulation sound, calling activity, call length, fundamental frequency, dominant frequency, acoustic communication, global warming, temperature
Journal Pre-proof Introduction Temperature plays a role when ectothermic animals such as insects, fish and amphibians communicate acoustically. Temperature effects are known on hindbrain central pattern generators controlling the activity of sonic muscles as well as on sensory organs and behaviour (Brenowitz et al., 1985; Bass and Baker, 1991; Gerhardt and Huber, 2002; Bass et al., 2015; Ladich, 2018). Fishes have probably evolved the largest diversity of sound-generating mechanisms (sonic organs) among vertebrates. According to the morphological structures involved, sonic organs may be classified into swim bladder, pectoral and head mechanisms (Ladich and
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Winkler, 2017). Swim bladder mechanisms are the most common and are based on fast-
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contracting muscles termed drumming (or vocal, or sonic) muscles that vibrate the swim bladder rapidly (Ladich and Bass, 2011; Ladich, 2014). Typically, one muscle contraction
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produces one sound pulse in single contraction calls, and the number of muscle contractions
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per second (muscle contraction rate) equals the fundamental frequency of long duration tonal drumming sounds composed of multiple contractions. The swim bladder muscles may be
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subdivided into intrinsic and extrinsic types, which refers to the fact that the drumming muscles are either entirely attached to the swim bladder or originate on additional structures
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such as bones (Ladich and Fine, 2006). The following sentence needs improving: Despite the many descriptions of sound-producing mechanisms, it is unknown how many of the 30,000+
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extant fish species emit acoustic signals for communication (Nelson et al., 2016). Cartilaginous species and many bony fishes lack sonic organs and are not known to
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communicate acoustically. Surprisingly, even closely related species such as representatives of Scorpaenidae (rockfishes) or Serrasalmidae (piranhas) evolved a diversity of mechanisms or may not be vocal (Hallacher, 1974; Melotte et al., 2019). Some fish species even possess two sound-generating mechanisms, enabling them to produce sounds covering different frequency ranges, typically a low-frequency and a highfrequency sound type. Representatives of several catfish families such as pimelodids, doradids, ariids and mochokids evolved various drumming muscles vibrating the swimbladder and a pectoral stridulatory mechanism (Fine and Ladich, 2003; Ladich and Bass, 2011; Ladich and Fine, 2006). The former muscles result in the emission of low-frequency drumming sounds with main energy below 500 Hz (Ladich et al., 1997). The latter mechanisms consist of enhanced first pectoral fin rays, termed pectoral spines, whose basal, ridged process rubs in a groove of the shoulder girdle and produces series of broadband pulses with main energy extending up to several kilohertz (Ladich, 1997; Papes and Ladich, 2011). Seahorses represent
Journal Pre-proof a second group of fishes emitting low-frequency drumming sounds (generated by an unknown mechanism) and high-frequency click sounds generated by rubbing two occipital bones (Colson et al., 1998; Oliveira et al., 2014). Temperature can affect sound production in fishes in several ways. First, it may change the calling activity, namely the number of sounds emitted in a certain time period. To study the effects of temperature on calling activity in the field is challenging. Additional ecological factors such as season, daily and lunar rhythms or water depth may influence calling (reviewed by Ladich, 2018). Under controlled laboratory conditions, contrasting results have been reported: no dependency of calling activity on temperature (juvenile grey
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gurnards Eutrigla gurnardus, Triglidae) versus an increase with temperature (juvenile Jarbua
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terapon Terapon jarbua, Terapontidae) (Schneider, 1964; Amorim, 2005). This is mirrored in field studies on the oyster toadfish Opsanus tau (Batrachoididae), some of which showed an
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increase of sound production with temperature, others no such effect (Fine, 1978; Montie et
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al., 2015, Ricci et al., 2017, Van Wert et al., 2019). This demonstrates that additional ecological constraints influenced calling activity.
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Beyond affecting calling activity, ambient temperature may influence the temporal and spectral characteristics of acoustic signals. The former includes sound duration, pulse periods,
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pulse repetition rates, fundamental or dominant frequencies of sounds, and perhaps sound levels. Those sound properties that directly depend on fast muscle contractions will be more
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affected by temperature than others. This is particularly the case in swim bladder drumming sounds generated by fast contractions of drumming muscles (Fine, 1978; Ladich, 1997;
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Connaughton et al., 2000; Amorim et al., 2006). The situation is very similar in gobies (Gobiidae), even though sounds are produced by a pectoral sonic muscle (Torricelli et al., 1990; Vincente et al., 2015; Parmentier et al., 2013, 2017). Generally, the drumming muscle contraction rate (pulse repetition rate, fundamental frequency) of drumming sounds increases with temperature. The situation is more complex in species emitting broadband pectoral sounds. Pulse periods may decrease when temperature increases, such as in the croaking gourami Trichopsis vittata (Ladich and Schleinzer, 2015). Elsewhere, no clear effects of temperature of the stridulatory sounds were reported, e.g. in the Striped raphael catfish Platydoras armatulus (Papes and Ladich, 2011). Mohajer et al. (2015) hypothesized that the frequencies of stridulatory sounds are primarily determined by inherent properties of the pectoral girdle in the blue catfish Ictalurus furcatus The present study is designed to investigate the effects of temperature on (1) calling activity and (2) temporal and spectral characteristics of sounds as well as (3) to address the
Journal Pre-proof question to which degree temperature differently affects sounds produced by two sonic mechanisms. A representative of the Amazonian catfish family Pimelodidae was chosen because it readily emits both types of sounds under hand-held conditions. Together with the known effects of temperature on hearing in P. pictus (Wysocki et al., 2009), the results shed some light on the potential influence on global warming on sound communication in fishes. Methods Animals Fifteen juvenile Pictus cats Pimelodus pictus (Pimelodidae) were investigated during this study (see Table 1 for size of fish). Sexing was not possible without killing the animals. They
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were kept in a community tank (100 x 50 x 50 cm) equipped with a layer of sand, roots,
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flower pots and plants as hiding places in a 12-h light – 12 h dark cycle. Fish were fed chironomid larvae except on recording days. The water temperature was controlled by
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submersible heaters and a water cooler (Hailea HC-250A) connected to an external filter.
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Sound Recording
The temperature in the community tank was increased or decreased by 1°C per day until the
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final temperatures were achieved. Fish were acclimated to these experimental temperatures for at least 3 weeks, first to 30°C, then to 22°C and finally again to 30°C.
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Sound recordings were conducted in a round plastic tub (35 cm diameter, 15 cm height, lined on the inside by acoustically absorbent material and a layer of fine sand). The
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water temperature was either 30 ± 1°C or 22 ± 1°C. Catfish were hand-held at a distance of 3 to 5 cm from the hydrophone, which was positioned in the middle of the recording tank. In
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order to avoid overlap of stridulation sounds generated simultaneously by both pectoral fins, one fin was fixed with a finger.
Sounds were recorded using a hydrophone (Brüel & Kjaer 8101) connected to a microphone power supply (Brüel & Kjaer 2408) which was connected to an external sound card (Edirol UA 25EX) of a laptop (Getac 300 B). The laptop ran Cool Edit 2000 (Syntrillium Software Corporation, Phoenix, AZ), and sounds were recorded at a sampling rate of 44.1 or 32 kHz. Sound Analysis Sounds were analyzed using Cool Edit 2000 and STX Sound Tools 3.7.8 developed by the Institute of Sound Research (Austrian Academy of Sciences, Vienna). All sound recordings were low pass filtered (5 kHz) to eliminate resonant frequencies using Cool Edit 2000. The following sound characteristics were determined in drumming and stridulation sounds. The calling activity represents the number of drumming or stridulation sounds
Journal Pre-proof produced within the first minute of sound recording, starting with the onset of the first sound. Duration of drumming and stridulatory sounds (ms) is the time between the onset of the first pulse until the end of the last. Fundamental frequency of drumming sounds (Hz) represents the frequency of lowest (1st ) harmonic. Dominant frequency (kHz) of stridulation sounds is the frequency with the highest amplitude (Fig. 1). Frequencies were measured using power spectra generated in STX (filter bandwidth 10 Hz, overlap 75 %, hanning filter).
Statistics Sound characteristic of 1 to 15 sounds per signal type were measured per specimen and the
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means calculated. These means were then used for further statistics. All data were tested for
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normal distribution using the Shapiro-Wilk test. When data were normally distributed, parametric statistical tests were applied, in other cases non-parametric tests were used.
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Because fish could be individually recognized based on the patterns of their spots, a repeated
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measures (RM) general linear model (GLM, ANOVA) was calculated followed by a Bonferroni post hoc test. If data were not normally distributed, a Friedman test was followed
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by a Dunn-Bonferroni post hoc test to reveal differences between temperatures. All statistical tests were run using IBM SPSS Statistics Version 26.
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Ethical considerations
All applicable national and institutional guidelines for the care and use of animals were
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followed (permit number BMWFW-66.006/0035-WF/V/3b/2017 by the Austrian Federal
Results
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Ministry of Science, Research and Economy).
Drumming and stridulation sounds Pictus cats produced drumming and stridulation sounds either separately from each other or at the same time. The drumming sound consisted of a series of low-frequency pulses with a rather constant pulse period, yielding harmonic sounds. The main energy of drumming sounds was concentrated in the fundamental frequency (1st harmonic) at approximately 120 to 200 Hz or in the second harmonic (Fig. 1, Fig. 2a, b). The drumming sound may consist of (a) a series of pulses of very similar amplitude, resulting in a long continuous drumming sound (Fig. 2a) or of (b) a series of short drumming sounds (bursts) or (c) of various intermediate stages. Figure 2b shows a series of 11 short drumming sounds of which the fourth, fifth and sixth merge into one another. Stridulation sounds are produced during abduction of pectoral spines in Pictus cats. In contrast to drumming sounds, they were built up of a series of short broadband pulses with
Journal Pre-proof main energies concentrated between 1 and 3 kHz (Fig. 3). Thus, main energies were clearly higher than in drumming sounds (Fig. 1, 4). The intervals between pulses were not as regular as in drumming sounds but varied considerably. Rather, they were typically large in the middle part of the sounds and small toward the beginning and end of the sounds (Figs. 3, 4). Size and calling activity Fish weight changed significantly over the course of experiments (RM-GLM: F2, 28 = 45.76, p < 0.001). Bonferroni post hoc tests revealed that fish gained weight between the first and second measurement but not between the second and third (Table 1). Nonetheless, changes in sound characteristics were independent of changes in body weight.
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The number of sounds produced by specimens within the first minute of sound
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recording ranged from no sounds to 71 in drumming sounds and from no sounds to 60 in stridulation sounds. The calling activity did not change with temperature either in drumming
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sounds (Friedman’s test: Chi-Square = 0.964, N = 15, df = 2, n.s.) or in stridulation sounds
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(Friedman’s test: Chi-Square = 5.193, N = 15, df = 2, n.s.) (Table 1). Temporal sound characteristics
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Both sound types of Pictus cats were longer at the lower temperature. The mean length of drumming sounds of specimen over all experiments ranged from 77.7 ms to 560 ms and
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increased significantly at 22°C (RM-GLM: F2, 24 = 16.56, p < 0.001) (Fig. 5a). Bonferroni post hoc tests revealed no difference between the 30°C measurements.
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Stridulation sounds were also shorter at 30°C than at 22°C (RM-GLM: F2, 18 = 29.28,
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p < 0.001) (Fig. 5a). The mean individual duration ranged from 23 ms to 103 ms over all experiments. Bonferroni post hoc tests revealed no difference between sounds produced at the 30°C measurements. Stridulation sounds were shorter than drumming sounds at all temperatures (Paired-samples T-test: 30°C: t = 6.94, df = 12, p < 0.001; 22°C: t = 12.80, df = 12, p < 0.001; 30°C repeated: t = 6.04, df = 12, p < 0.001) (Table 1). Table 1. Mean (± S.E.) body weight, calling activity (number of sounds) and sound characteristics of drumming (DR) and stridulation sounds (SR) of Pictus cats at the experimental temperatures. The range is given in brackets. The second number in brackets gives the number of sound-producing individuals.
Variable
Body weight (g)
30°C
22°C
30°C
3.61 ± 0.14
4.54 ± 0.14
4.80 ± 0.22
(2.5 - 4.5)
(3.5 - 5.6)
(3.43 - 6.12)
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Sound duration DR (ms)
Sound duration SR (ms)
Fundamental frequency DR (Hz)
10.20 ± 1.82
9.27 ± 1.76
(1 - 71; 15)
(0 - 28; 14)
(0 - 24; 14)
9.40 ± 2.74
17.67 ± 3.24
12.0 ± 3.84
(0 - 34; 13)
(0 - 40; 13)
(0 - 60; 13)
241.6 ± 25.1
437.1 ± 23.3
273.8 ± 37.9
(77.7 - 408.5)
(231.9 - 600.1)
(109.2 - 559.6)
39.49 ± 3.44
83.17 ± 3.59
39.41 ± 3.32
(23.0 - 68.0)
(61.9 - 103)
(19.3 - 64.9)
220.2 ± 3.60
142.7 ± 2.53
212.8 ± 2.46
(190.6 - 242.2)
(126.7 - 156.3)
(186.2 - 225.0)
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Sound number SR
14.53 ± 4.66
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Sound number DR
2.512 ± 134 Dominant frequency SR (kHz)
2.274 ± 100
2.154 - 2.793)
(1.666 - 2.957)
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(1.912 - 3.391)
2.508 ± 51
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Spectral characteristics of sounds
The fundamental frequency of drumming sounds differed significantly with temperature
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(Friedman’s test: Chi-Square = 20.46, N = 13, df = 2, p < 0.001). The mean fundamental frequency ranged from 127 Hz to 242 Hz. Dunn-Bonferroni post hoc tests revealed that the
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fundamental frequency is lower at 22°C than at both 30°C measurements (Fig. 6a). The dominant frequency of stridulation sounds also differed between experiments
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(RM-GLM: F2, 18 = 6.663, p < 0.007), with mean individual frequencies ranging from 1.67
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kHz to 3.40 kHz. Bonferroni post hoc tests revealed no difference between the sounds recorded in the first experiment at 30°C and those recorded at 22°C on the second trial. There was a difference between sounds emitted at 22°C and those produced on the third attempt at 30°C (Fig. 6b). Thus, there is no clear temperature effect on the dominant frequencies of stridulation sounds. Discussion Sound production during hand-held conditions has been frequently described in fishes (e.g. Salmon, 1967; Ladich, 1997; Heyd and Pfeiffer, 2000; Melotte et al., 2016). The emission of sounds in distress situations including sounds uttered when predators approach or even grab prey fish raises the question on its functional significance. So far no evidence is available to suggest that such fish try to warn conspecifics or successfully deter predators (Markl, 1968; Myrberg, 1981;, Bosher et al., 2006; Bessey and Heithaus, 2013). Our current lack of information, however, does not exclude that sound production under these conditions is a means of intra- or interspecific acoustic communication.
Journal Pre-proof Calling activity The number of sounds (drumming and stridulation sounds) produced by Pictus cats did not depend on temperature in the present study. Numerous field and lab studies have investigated the effects of temperature on fish vocalizing activity (Ladich, 2018). Despite the wide variety of experimental setups and species chosen, no clear temperature effect on calling activity was found. Laboratory studies can control various parameters such as the light cycle, making it easier to describe solely the influence of temperature on sound production. In the lab, for example, an increase in calling activity with temperature was described in the gudgeon Gobio gobio (Cyprinidae), the Jarbua terapon Terapon jarbua (Terapontidae),
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the bullhead Cottus gobio (Cottidae) and the red drum Sciaenops ocellatus (Sciaenidae)
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during seasonal light regimes or 12h:12h light cycles (Schneider, 1964; Ladich, 1988; 1989, Montie et al., 2016). In contrast, no such temperature effects were observed in the painted
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goby Pomatoschistus pictus (Gobiidae), the grey gurnard Eutrigla gurnardus (Triglidae) and
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the Atlantic cod Gadus morhua (Gadidae) (Brawn, 1961; Amorim, 2005; Vicente et al., 2015).
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In field studies as well, both an increase in calling activity with temperature and no effect have been reported even in the same species. This is less of a surprise considering the
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large number of factors involved besides temperature. For example, the number of individuals calling on different recording days remains unknown. In the frequently investigated oyster
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toadfish, conflicting results are reported. Montie et al. (2015) noted an increase in the number of boatwhistles — the advertising calls of the oyster toadfish — in the May River, South
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Carolina, whereas no such correlations to temperature were described by others, although seasonal, lunar and daily calling rhythms were distinguished (Monczak et al., 2017; Ricci et al., 2017). Amorim et al. (2006) observed a seasonal increase in calling activity with temperature
in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae) in the Tagus estuary, Portugal, and a drop in sound production in late July at high temperatures. Furthermore, water depth may affect calling. A seasonal increase in sound production was reported in the spotted weakfish Cynoscion nebulosus (Sciaenidae), particularly in deeper water (Montie et al. 2015). In summary, calling activity apparently increases with temperature in most species, parallel to a general increase in agonistic and reproductive behaviour. The lack of a temperature effect in this parameter, such as in the Pictus cat, may have numerous reasons. One might be the behavioural context: distress situations, for example, are not necessarily related to reproductive behaviour. Another potential explanation is that distress levels vary considerably between individuals, which could mask a significant difference between
Journal Pre-proof temperatures. In the Pictus cat, the number of drumming sounds emitted within the first minute on the first recording day varied from 1 to 71 between individuals. Similarly, Fine and Waybright (2015) reported that the number of grunts in a train and other sound properties were highly variable in oyster toadfish when specimens were recorded twice. Temporal characteristics The duration of both sound types was clearly temperature-dependent in the Pictus cat. Drumming and stridulation sounds were about half as long at 30°C as at 22°C. This can be explained by higher firing rates of central pattern generators und subsequently faster contractions of muscles at the higher temperature (Bass et al., 2015). A similar observation
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was made for the pectoral sounds in Platydoras armatulus and Trichopsis vittata (Ladich and
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Schleinzer, 2015). In P. armatulus, stridulation sounds emitted both during abduction and adduction of the large pectoral spines were shorter at 30°C than at 22°C (Papes and Ladich,
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2011)
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The duration of drumming sounds was clearly temperature-dependent in Pictus cats, but no such effect was observed in other species such as in P. armatulus sounds recorded in
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the same behavioural context or in the mating calls of the oyster toadfish (Fine, 1978; Papes and Ladich, 2011). The shorter total duration in the Pictus cat may partly be explained by
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faster muscle contraction – as long as the number of muscle contractions is similar at all temperatures (as is the case in stridulation sounds, where the number of pulses is largely
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limited by the number of ridges on the proximal end of the pectoral spine) (Fine and Ladich 2003). However, the number of muscle contractions and thus pulses is not limited in
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drumming sounds, helping to explain why potential temperature effects on sound length may be missing (Fine, 1978). There is evidence that separate pattern generators in the hindbrain code the pulse repetition rate (fundamental frequency) and call duration in fishes (Bass et al., 2015). Vocal pacemaker nuclei (VPN) determine the pulse repetition rate, whereas vocal prepacemaker (VPP) neurons determine the duration of calls. The effect of temperature on sound duration is even more complex. In the Pictus cat, drumming and stridulation sounds became shorter at 30°C even though they are being produced by different sonic mechanisms in the same (distress) context. In contrast, opposite effects may be observed in different behavioural contexts in sounds produced by the same sonic organs within a species. Amorim et al. (2006) described an increase in the duration of boatwhistles, the mating signal of the toadfish H. didactylus, which are produced by their intrinsic swimbladder muscles. At the same time, Amorim et al. (2006) observed a decrease in the duration of croaks, an agonistic call.
Journal Pre-proof Spectral characteristics of sounds The fundamental frequency of drumming sounds in Pictus cats increased significantly with ambient temperature. The fundamental frequency or pulse repetition rate of drumming sounds is the sound property most regularly affected by temperature. This effect has been demonstrated in nearly all studies investigating temperature effects on sound production in fishes such as toadfishes, piranhas, searobins, gobies, drums, etc. (Fine, 1978; Kastberger 1981; Brantley and Bas,s 1994; Lugli et al., 1996; Connaughton, 2004; Connaughton et al., 2002; Maruska and Mensinger, 2009, Ladich, 2018). The increase in fundamental frequency demonstrates the importance of temperature on the firing rate of central pattern generators and
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on sonic muscle contraction rates.
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In contrast, the dominant frequency of pectoral stridulation sounds shows no clear difference between temperatures, similarly to the fundamental frequency, and seems to be
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independent of temperature. This can partly be explained by the difficulty in measuring the
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dominant frequency of a stridulation sound. The sound energy is broadly distributed within a stridulation sound, and main energies may in addition switch in frequency range between
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adjacent pulses within a stridulation sound (see sonagrams). This complicates determining the frequency with the highest amplitude. Accordingly, the mean dominant frequency varied
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considerably between individual fish within one measurement, ranging from 1912 Hz to 3174 Hz at the first 30°C measurement.
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A lack of a temperature dependency of dominant frequencies was also observed in a prior study on doradid stridulation sounds. In P. armatulus, Papes and Ladich (2011)
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described differences in the dominant frequency when shifting from 22°C to 30°C but not from 30°C to 22°C when the lower temperature experiments were repeated. In contrast, the dominant frequency of croaking sounds in the gourami T. vittata was affected by temperature. Ladich and Schleinzer (2015) observed an increase from 1221 Hz at 25°C to 1270 Hz at 30°C to 1341 Hz at 35°C. The dominant frequency was lower at the first two temperatures as compared to the highest one. These differences between catfishes and croaking gourami most likely reflect their different sound-generating mechanisms. Trichopsis vittata produces pectoral sounds by plucking enhanced tendons in its pectoral fins, whereas catfishes rub their pectoral spines in the pectoral girdle (Fine and Ladich, 2003; Ladich and Fine, 2006). The dominant frequency of croaking sounds in T. vittata seems to be based on to the speed of pectoral muscle contractions and on the resonances of their air-breathing cavity (suprabranchial air-breathing organ) adjacent to the pectoral girdle. In catfishes the frequency spectrum appears to be determined primarily by the pectoral girdle, not by the swimbladder.
Journal Pre-proof Fine et al. (1997) removed the air in the swimbladder of the channel catfish Ictalurus punctatus and found that the frequency spectra were similar before and after deflation, indicating that the swimbladder plays no major role in determining the sound frequency. Mohajer et al. (2015) demonstrated that different pectoral fin speeds resulted in a rather similar frequency spectrum, indicating that the spectrum is dictated primarily by the natural frequency of the pectoral girdle. Thus, a strong temperature effect on pectoral sounds cannot be expected. Did significant changes in fish size during the course of the experiments effect sound characteristics in the Pictus cat? None of the determined sound properties changed in parallel
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with body weight. Neither the lack of a change in calling activity, the decrease in call lengths
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nor the increase in fundamental frequency were paralleled by changes in body size. Conclusion
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The current study reveals that ambient temperature does not affect acoustic signals produced
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by fundamentally different sonic mechanisms in the same ways within one species. The number of drumming and stridulation sounds produced by the Pictus cat does not depend on
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temperature. This may be explained by the fact that both sounds were emitted in the same behavioural context and that the fish may be similarly stressed at both temperatures. The
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shorter duration of both sound types at the higher temperature is due to the central pattern generators and thus higher speed of swimbladder and pectoral muscle contractions at 30°C.
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Finally, we attribute the differences in temperature dependency of the spectral characteristics of sounds (fundamental and dominant frequency) to the fundamental difference in sound-
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generating mechanisms.
Despite differences in the properties of low- and high-frequency sounds, ambient temperature clearly affected acoustic signaling in the Pictus cat. This is paralleled by temperature-dependent differences in hearing (Wysocki et al., 2009). The Pictus cat is more sensitive at higher temperatures. We currently know next to nothing about whether the changes in sound characteristics are coupled to temperature-dependent changes in hearing sensitivities in fishes, as is the case in frogs (Gerhardt, 1978). One study in the midshipman Porichthys notatus indicates that such a phenomenon exists in fishes (McKibben and Bass, 1998). The temperature dependency of acoustic signaling and hearing sensitivity, and of the potential coupling between both, raises the question whether global warming affects sound communication in fishes. Narins and Meenderink (2014) predict that ongoing temperature change will effectively uncouple the sound production and detection systems in frogs,
Journal Pre-proof affecting acoustic communication negatively. We expect similar developments in vocal fish taxa. Acknowledgements We thank Min Chai, Joana Schär and Sandra Weber for their help in collecting data, Michael Stachowitsch for scientific English proofreading and two reviewers for helpful comments. This study was supported by the Austrian Science Fund (FWF grant no. P31045). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Conflict of Interests The authors declare no conflict of interest. Supplementary material
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S1: Recording of a long drumming sound of a Pictus cat illustrated in figure 2a. S2: Recording of a series of 11 short drumming sounds illustrated in figure 2b.
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S3: Recording of three stridulation sounds illustrated in figure 3. S4: Recording of a drumming and stridulation sound emitted simultaneously and illustrated in
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figure 4. References
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Narins, P. M. and Meenderink, S. W. F. (2014). Climate change and frog calls: long-term correlations along a tropical altitudinal gradient. Proceedings of the Royal Society B, Biological Sciences 281: 20140401. Nelson, J. S., Grande, T. C. and Wilson, M. V. H. (2016). Fishes of the World. (5 edn). Hoboken, New Jersey: John Wiley & Sons, Inc. Oliveira, T. P. R., Ladich, F., Abed-Navandi, D., Souto, A. S. and Rosa, I. L. (2014). Sounds produced by the longsnout seahorse: a study of their structure and functions. Journal of Zoology 294: 114-121.
Journal Pre-proof Papes, S. and Ladich, F. (2011). Effects of temperature on sound production and auditory abilities in the Striped Raphael Catfish Platydoras armatulus (Family Doradidae). PLoS ONE 6: e26479. Parmentier, E., Kéver, L., Boyle, K., Corbisier, Y.-E., Sawelew, L. and Malavasi, S. (2013). Sound production mechanism in Gobius paganellus (Gobiidae). The Journal of Experimental Biology 216: 3189-3199. Parmentier, E., Petrinisec, M., Fonseca, P. J. and Amorim, M. C. P. (2017). Sound-production mechanism in Pomatoschistus pictus. Journal of Experimental Biology 220: 4374-4376. Ricci, S. W., Bohnenstiehl, D. R., Eggleston, D. B., Kellogg, M. L. and Lyon, R. P. (2017).
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oyster restoration site. PLOS ONE 12(8): e0182757.
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Oyster toadfish (Opsanus tau) boatwhistle call detection and patterns within a large-scale
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Pacific Science 11: 364-381.
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Schneider, H. (1964). Physiologische und morphologische Untersuchungen zur Bioakustik der Tigerfische (Pisces, Theraponidae). Zeitschrift für vergleiche nde Physiologie 47: 493-558.
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Torricelli, P., Lugli, M. and Pavan, G. (1990). Analysis of sounds produced by male Padogobius martensi (Pisces: Gobiidae) and factors affecting their structural properties.
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Bioacoustics 2(4): 261-276.
Van Wert, J. C. and Mensinger, A. F. (2019). Seasonal and daily patterns of the mating calls
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of the oyster toadfish, Opsanus tau. The Biological Bulletin: doi: 10.1086/701754. Vicente, J. R., Fonseca, P. J. and Amorim, M. C. P. (2015). Effects of temperature on sound
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production in the painted goby Pomatoschistus pictus. Journal of Experimental Marine Biology and Ecology 473: 1-6.
Wysocki, L. E., Montey, K. and Popper, A. N. (2009). The influence of ambient temperature and thermal acclimation on hearing in a eurythermal and a stenothermal otophysan fish. Journal of Experimental Biology 212: 3091-3099. Figure legends Fig. 1. Sound spectrum of a drumming- and a stridulation sound emitted simultaneously (see also Fig. 4) by a Pictus cat showing the difference in energy content of both sound types and frequencies measured. The fundamental frequency (FF) was determined in drumming sounds and the dominant frequency (DF) in stridulation sounds. Note the harmonic content of the drumming sound with the fundamental frequency and the second harmonic (asterisk) containing the highest energy. Sampling frequency 44.1 kHz, filter bandwidth 10 Hz, overlap 75%, hanning window.
Journal Pre-proof Fig. 2. Sonagram and oscillogram of (a) a long, continuous drumming sound and (b) a drumming sound consisting of a series of 11 short drumming sounds (bursts) emitted by a Pictus cat. Note in (b) that short bursts 4, 5 and 6 are not clearly separated. Sampling frequency 44.1 kHz, filter bandwidth 25 Hz, overlap 75%, hanning window. Fig. 3. Sonagram and oscillogram of three stridulation sounds emitted independently from drumming sounds by a Pictus cat. Note that the main sound energies are located between 1 and 3 kHz. Sampling frequency: 32 kHz, filter bandwidth 225 Hz, overlap 75%, Hanning filter. Fig. 4. Sonagram and oscillogram of a drumming sound and a stridulation sound produced
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simultaneously by a Pictus cat, illustrating the difference in sound length and frequency
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content. Note that the difference in drumming sounds shown in Fig. 2 and Fig. 4 is due to different filter bandwidth. Sampling frequency 44.1 kHz, filter bandwidth 250 Hz, overlap
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75%, hanning window.
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Fig. 5. Mean (+ S.E.) (a) duration of drumming sounds at different temperatures and of (b) stridulation sounds at different temperatures. Different letters above bars indicate significant
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differences between temperatures (P < 0.05).
Fig. 6. Mean (+ S.E.) (a) fundamental frequency of drumming sounds at different
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temperatures and (b) dominant frequency of stridulation sounds at different temperatures.
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Graphical abstract
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Different letters above bars indicate significant differences between temperatures (P < 0.05).
Journal Pre-proof Highlights (Bullet points) Acoustic signaling in fishes is variously influenced by ambient temperature. Pictus catfish emit low-frequency drumming and high- frequency stridulation sounds. Number of emitted drumming and stridulation sounds did not change with temperature. Temporal sound characteristics were similarly, spectral properties differently affected. Temperature effects depend on sound characteristic and sonic mechanism in Pictus
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cats.
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