Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE Passive acoustic recording of Ophidion rochei calling activity in Calvi Bay (France) Lo€ıc Kever 1, Pierre Lejeune2,Lo€ıc N. Michel2,3 & Eric Parmentier1
1 Laboratoire de Morphologie Fonctionnelle et Evolutive, AFFISH, Institut de chimie, UniversitedeLi ege, Liege, Belgium 2 STARESO Research Station, Revellata Cape, Calvi (Corsica), France 3 Laboratory of Oceanology, MARE Center, University of Liege, Liege, Belgium
Keywords Abstract Biological cycle; fish; Ophidiiformes; sound production. Passive acoustic recording (PAR) systems are non-invasive and allow research- ers to collect data over large spatial and/or temporal scales. As fish sounds are Correspondence species-specific and repetitive, PAR can provide a large amount of data about Lo€ıc Kever, Laboratoire de Morphologie spatio-temporal variation in fish distribution and behaviors. Ophidion rochei, Fonctionnelle et Evolutive, AFFISH, Institut de found in the Mediterranean and Black Seas, is a sand-dwelling species, meaning chimie, Baˆ timent B6c, UniversitedeLiege, that the behavior of this cryptic nocturnal fish cannot be observed in the field. B-4000 Liege, Belgium. Fortunately, male O. rochei produce long, multiple-pulsed calls that are easy to E-mail: [email protected] identify. The aim of this study was to determine whether or not male calls are Accepted: 31 August 2015 linked to reproduction behaviors. If so, PAR would allow a detailed description of the seasonal and daily rhythms in O. rochei reproduction behavior. A hydro- doi: 10.1111/maec.12341 phone was deployed from 18 July 2011 to 21 June 2012 and from 7 June 2013 to 2 July 2013 on a sandy area (42°3404800 N, 8°4304300 E) in front of the STARESO research station (NW Corsica). Male sounds were obtained only at night from late spring to early fall. The annual sound production period corre- sponds to the reproductive season of O. rochei. Sound production followed diel cycles: it was sustained for the entire night at the beginning of the sound pro- duction season but limited to shorter periods in the evening during the second half of the season. These differences in daily and seasonal sound production tempo can be used in future recordings to make inter-annual comparisons and estimate the physiological state of the fish.
them (e.g. Lobel 1992; Brantley & Bass 1994; Mann & Introduction Lobel 1998; De Jong et al. 2007; Parmentier et al. 2010a, Passive acoustic recording (PAR) systems are key tools to b; Colleye & Parmentier 2012). In addition, some species improve our knowledge in diverse fields of marine biol- are known to produce different kinds of sounds depend- ogy. These techniques are non-invasive and allow ing on the fish behavior (e.g. Gray & Winn 1961; Lugli researchers to collect data over large spatial and/or tem- et al. 1997; Mann & Lobel 1998; Parmentier et al. 2010a). poral scales (Wall et al. 2012, 2013). Moreover, they are As fish sounds are species-specific and repetitive, PAR appropriate for collecting data at night or in dark envi- can provide a large amount of data about spatio-temporal ronments, such as caves and the deep sea, because they variation in fish distribution and behavior (Mann & are not constrained by the amount of available light. Grothues 2009; Wall et al. 2012). Despite numerous During the last several decades, sounds have been behaviors being associated with sound production in recorded from numerous fish species (Slabbekoorn et al. fishes, most of the sounds are closely or indirectly related 2010; Fine & Parmentier 2015) and specific behaviors to behaviors associated with reproduction: territoriality related to these sounds have been described for many of (e.g. Takemura 1984; Tricas et al. 2006; Parmentier et al.
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2010a), mate courting (e.g. Tavolga 1958; Mann & Lobel female sounds are short with a regular, short duration 1998; Amorim et al. 2003), gamete release (e.g. Lobel pulse period while male sounds (Fig. 1) are much longer, 1992; Hawkins & Amorim 2000; Ladich 2007) and paren- pulsed and show a unique pulse period pattern (K ever tal care (e.g. Longrie et al. 2013). Disturbance calls, by et al. 2012). contrast, have often been reported in captivity but are The biology of O. rochei is still poorly documented, uncommon under natural conditions (Ramcharitar et al. mainly because of its burrowing behavior and nocturnal 2006). way of life, which complicate or prevent direct observa- As sounds are associated with reproductive behavior in tion. Here, we took advantage of the benefits (i.e. oppor- many fish species, spawning season is often paralleled by tunity to study animal behavior during long time periods an increase in calling events (e.g. Brawn 1961; Fish & and at high temporal resolution) of PAR to investigate Cummings 1972; Locascio & Mann 2011). Sound produc- temporal variation of activity periods of male O. rochei tion also varies throughout spawning season; diel cycles throughout the year. Moreover, hypothesizing that sound are generally notable and acoustic activity of many species production is related to reproduction-associated behav- peaks at dusk and/or at dawn (e.g. Mann & Lobel 1995; iors, we explored links between environmental factors Boyle & Tricas 2010; Parmentier et al. 2010b; Longrie such as photoperiod and seawater temperature and the et al. 2013). In some species, it is also affected by other timing of reproduction onset and end-point. All these factors such as moon phases (Mann et al. 2008). data on the cryptic O. rochei will provide precious infor- Photoperiod is generally considered to be the main mation to plan future field studies. environmental factor that determines the onset and dura- tion of reproductive period in fishes (Bromage et al. Material and Methods 2001; Pankhurst & Porter 2003; Migaud et al. 2010). However, the roles of many other factors have also been Recordings of Ophidion rochei sounds demonstrated (Bromage et al. 2001; Pankhurst & Porter 2003; Clark et al. 2005; Migaud et al. 2010). Environmen- A digital spectrogram long-term acoustic recorder (DSG; tal temperature is an important criterion, especially in Loggerhead Instruments, Sarasota, FL, USA) was poikilotherms, notably because of its effects on the gona- deployed during two field campaigns in order to provide dal maturation (Hutchings & Myers 1994) and the neu- the equivalent of a complete year of recording. During romotor system (Walker 1975). the first campaign, the DSG ( 186 dB re 1 V lPa 1, Ophidion rochei Muller,€ 1845, is a sand-dwelling species 1 dB from 20 Hz to 20 kHz) was deployed almost con- from the Mediterranean and Black Seas (Jardas 1996; tinuously from 18 July 2011 to 21 June 2012 (see Fig. 2A Matallanas & Casadevall 1999). It is found at depths for more details about the actual recording periods). It ranging from a few meters to 150 m, is active at night was positioned at a depth of 40 m, on the sea floor in a and reproduces from June to September (Jardas 1996). In sandy area located in front of the STARESO station this species, both sexes are able to produce sounds; (42°3404800 N, 8°4304300 E; Fig. 3), Corsica. Because of storage limitations, the DSG was programmed to record 5 min per hour at a sample rate of 20 kHz for durations of approximately 3 months, after which the recorder was removed and redeployed two times (see Fig. 2A) by SCUBA divers. During the first year of recording, the hydrophone was not deployed during late June and early July. However, preliminary analyses suggested that this period corre- sponds to the sound production onset. Thus, a mini-DSG (Loggerhead Instruments) was deployed at the same loca- tion from 7 June 2013 to 2 July 2013 (Fig. 2A). It was also set to record 5 min per hour at 20 kHz. The hydro- phone on this device had a slightly higher sensitivity ( 180 dB re 1 V lPa 1).
Analyses of Ophidion rochei sounds Fig. 1. Waveform of a male Ophidion rochei call recorded in July 2011 in Calvi Bay (France). Gray: long pulse periods, white: short In order to extract Ophidion rochei sounds, all recordings pulse periods. were investigated in AVISOFT SAS-LAB PRO 5.2 (Avisoft
1316 Marine Ecology 37 (2016) 1315–1324 ª 2016 Blackwell Verlag GmbH Kever, Lejeune, Michel & Parmentier Ophidion rochei calling activity in Calvi Bay
Fig. 2. Seasonal variation in sound production of male Ophidion rochei in Calvi Bay (France). (A) Timeline showing the periods of actual recordings (light gray) from 1 July 2011 to 30 June 2012 and from the 1 June to 2 July 2013. No data were obtained for the time periods in dark gray. (B) Daily sound production of O. rochei averaged for each month of recordings. Means and standard deviations are shown. (C) Short (gray) and long (black) pulse periods averaged from 10 sounds for each month of recording. Means and standard deviations are shown except for June 2012 because a single sound was recorded during this month. A dashed gray line is drawn at 100 ms to facilitate comparisons.
Bioacoustics, Berlin, Germany). A signal was classified as Temporal variations of sound production a male O. rochei sound when it showed the same acoustic The analysis of recording frames was divided into two characteristics as the calls previously recorded for this steps. First, 2 days (day 1 and day 4 of the week) for each species (see Parmentier et al. 2010b; K ever et al. 2012, week of recording were examined in order to search for 2014). The identification is mainly based on the species- and identify every male call. These data allowed the deter- specific pulse period pattern with the pulse period pro- mination of the seasonal variations in sound production gressively increasing in the first part of the sound before using months as treatment groups. Second, for months alternating between long and short durations (Fig. 1). In actually showing Ophidion rochei sound production, each addition, we verified that pulses were dominated by two day of recording was investigated. This allowed the peak frequencies and that the values for pulse duration, description of daily cycles. In addition, the effect of the peak frequencies and pulse number were in the same moon on daily sound production was investigated. Each range as in our previous recordings of male O. rochei. lunar cycle was divided into four periods [new moon
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basis further out in Calvi Bay (42°3403400 N, 8°4404200 E; Fig. 3) using a SBE19 CTD probe (Sea-Bird Electronics, Bellevue, WA, USA). At this depth, no data were available for 2011.
Statistical analyses Statistical tests were performed in STATISTICA 10 (Stat- Soft Inc., Tulsa, OK, USA). Normal distribution of obser- vations was tested using Kolmogorov–Smirnov test (a = 0.05). Depending on the result, parametric [a t-test or a one-way analysis of variance (one-way ANOVA) fol- Fig. 3. Locations of sound and temperature recordings in Calvi Bay lowed by Tukey’s honest significant difference (HSD) (France). The Mediterranean Sea is in gray and Corsica in white. (1) – Location of temperature recordings at 3 m in STARESO harbor post-hoc tests] or non-parametric (Kruskal Wallis fol- 0 00 0 00 – (42°34 49 N, 8°43 28 E). (2) Location of sound recordings at 40 m lowed by Bonferroni-corrected Mann Whitney U-tests on a sandy area (42°3404800 N, 8°4304300 E), in front of the STARESO for multiple comparisons) tests were applied. station. (3) Location of temperature recordings at 40 m in Calvi Bay (42°3403400 N, 8°4404200 E). Results (NM) period: from NM 3 days to NM + 3 days; first Seasonal cycle quarter (FQ) period: from FQ 3 days to FQ + 3 days; full moon (FM) period: from FM 3 days to FM + 3 No female sounds were identified during field recordings days; last quarter (LQ) period: from LQ 3 days to in Corsica. No male sounds were recorded from Novem- LQ + 3 days] defined as treatment groups. ber 2011 to May 2012 (Fig. 2B). Only one sound was recorded in October 2011 (1 October) and another one Seasonal variations in pulse period in June 2012 (14 June). The single sound recorded in The long and short pulse periods (Fig. 1) were measured October was to weak to be analyzed properly. During for 10 calls per month because K ever et al. (2015) summer 2011, the sound production was significantly reported that Ophidion rochei pulse periods vary with sea- higher in July (one-way ANOVA, P < 0.05; Tukey’s HSD, water temperature. Months were defined as treatment P < 0.05,) with 17 5 sounds recorded per day groups and October 2011 and June 2012 were excluded (mean SD; Fig. 2B). As the hydrophone was set to from pulse period analyses because a single sound was record 5 min per hour, the same device set to record recorded for each of these months. Note that short and continuously would have recorded 200 calls per day. long pulse periods were measured several times in each There were at least two callers because some sounds par- sound but the averages calculated for each sound were tially overlapped. Although sound production in August used for the statistical analysis. and in September did not differ (Tukey’s HSD, P = 0.59), sound production declined gradually from July 2011 to the beginning of October 2011 (Fig. 2B). Recordings of seawater temperature In 2013, the recordings lasted from 7 June to 2 July. Seawater temperature at 3 m depth was recorded every Many more sounds were recorded than in June 2012 10 min in the harbor of the STARESO station (Fig. 2B): 470 sounds were recorded from 7 to 21 June (42°3404900 N, 8°4302800 E; Fig. 3), using a PT 100 probe 2013 while a single sound was obtained during that per- (Neotek, Caudan, France) connected to a HD 32.7 real- iod in 2012. Daily sound production (mean SD: time datalogger (Delta Ohm, Padova, Italy). When data 31 6 sounds) was also significantly higher (t-test, from the probe were not available due to instrument mal- P < 0.05) than in July 2011. No obvious trend in sound function (1 February 2012 to 20 February 2012 and 29 production was observed during this period and the slope May 2012 to 13 June 2012), data from a different sensor for sound number per day plotted against date (each day (MiniLog-T; Vemco, Bedford, Canada) located at the was labeled from 1 to 26) did not differ from 0 (linear same place and depth was used. In the present study, regression, r2 = 0.005 and P = 0.73). daily averages were computed on data recorded from 1 In 2012 and 2013, the sea surface temperature February 2012 to 1 October 2012 and from 1 February increased from February (approximately 13 °C) to August 2013 to 1 October 2013. During the same periods, tem- (approximately 25 °C) and decreased to approximately perature at a depth of 40 m was recorded on a weekly 22 °C at the end of September (Fig. 4A). At 40 m, the
1318 Marine Ecology 37 (2016) 1315–1324 ª 2016 Blackwell Verlag GmbH Kever, Lejeune, Michel & Parmentier Ophidion rochei calling activity in Calvi Bay
Fig. 4. Seawater temperature in Calvi Bay. (A) Sea surface temperature, measured in STARESO harbor (42°3404900 N, 8°4302800 E) and (B) seawater temperature measured at 40 m in Calvi Bay (42°3403400 N, 8°4404200 E). Gray lines and triangles: 2012, black lines and circles: 2013. Dashed lines indicate the period during which the temperature at 40 m was higher in 2013 than in 2012. lowest temperatures were also recorded in February time. Figure 5 investigates the relationships between the (approximately 13 °C). However, water temperature at photoperiod and daily cycle of sound production. This 4- 40 m increased later in the season, more slowly and less month period has been divided in five subperiods because regularly than at the sea surface (Fig. 4B). It only reached the photoperiod varied notably from June to September 20 °C in September 2012. During spring 2013, seawater at the study site: night-time lasts approximately 8 h in temperature at 3 m depth was higher than during spring early June and almost 12 h in late September. In Fig. 5, 2012 (Fig. 4A). At 40 m, it was also higher during late daily cycles with similar photoperiod were pooled April 2013 and the first half of May 2013 than at the together. For example, mean values presented in Fig. 5B same period in 2012 (Fig. 4B). By contrast, temperature correspond to all daily cycles when there were only 8 h at 40 m was lower during June 2013 compared with the of recordings between sunset and sunrise. same month in 2012 (Fig. 4B). During late spring and early summer (night-time: Despite mean values for both short and long pulse 21:00–05:00 and 22:00–05:00 h), sound production periods (Fig. 2C) being shorter in September 2011 lasted for the whole night duration and seemed to peak (103 17 ms, n = 10 and 132 21 ms, n = 10, respec- 2–3 h after sunset (Fig. 5A and B). A second peak was tively) than in July 2011 (122 15 ms, n = 10 also observed at the end of the night, 2 h before sunrise. and 151 19 ms, n = 10, respectively), August 2011 From mid-July to October (night-time: from 21:00–6:00 (123 6 ms, n = 10 and 153 8 ms, n = 10 respec- h to 20:00–07:00 h), the evening peak in sound produc- tively) and June 2013 (123 5 ms, n = 10 and tion was also observed approximately 2 h after sunset 148 7 ms, n = 10, respectively), a significant difference (Fig. 5C–E). However, after this peak, sound production (Bonferroni-corrected Mann–Whitney, P < 0.05) was was generally very low. In some cases, a morning peak only observed between the short pulse periods measured was visible 2–3 h before sunrise (Fig. 5C–E). in September and July 2011. Night-time was divided into three periods (evening Male sound production lasted from late spring to early period: sunset + 1 h and sunset + 2 h; night period: fall, with a peak in June or July and a sharp drop during sunset + 3 h to sunrise 3 h; morning period: sun- early fall. The short and long pulse periods were slightly rise 2 h and sunrise 1 h) used as treatment groups shorter in September, which is in accordance with the to test the significance of the variations observed in higher temperature recorded at 40 m during this month Fig. 5. During the first two photoperiods (night-time: (see: K ever et al. 2015). 21:00–05:00 and 22:00–05:00 h), sound production did not differ significantly between night periods (Kruskal– Wallis, respectively: P = 0.96 and P = 0.08). By contrast, Daily cycle sound production varied significantly (Kruskal–Wallis, Male Ophidion rochei calls were recorded only between P < 0.05) between some night periods during the three sunset and sunrise; no sounds were recorded during day- other photoperiods (night-time: 21:00–06:00, 20:00–06:00
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Fig. 5. Mean daily cycles in sound production of male Ophidion rochei in Calvi Bay (France). The period between June and September has been segmented into five intervals (A–E) according to the photoperiod. Symbols are in gray when recordings were performed during daytime and in black when they were performed during night- time. Means and standard deviations are shown.
and 20:00–07:00 h). In the three latter cases, only evening period differed (Bonferroni-corrected Mann–Whitney, P < 0.05) from the other night periods. In short, during the first part of the sound production period, males called all night long while later in the season (longer night-time) they produced sounds almost exclusively shortly after sunset.
Lunar cycle Sound production showed no obvious trend related to lunar cycles in 2011 and 2013 (Fig. 6) and no significant difference was found between the moon phases (one-way ANOVA, respectively: P = 0.09 and P = 0.21).
Discussion
Sound production and associated behavior Many male fish produce sound during behaviors associ- ated with reproduction (Tavolga 1958; Guest & Laswell 1978; Mann & Lobel 1998; Amorim et al. 2003; Par- mentier et al. 2010a). The multiple-pulsed sounds of male Ophidion rochei are produced at night from June to early October. According to Jardas (1996), the reproductive period of this species lasts from June to September. Casadevall (1991) observed a high gonado- somatic index in both sexes for the same period and suggested a peak in sperm emission during September. The sound production season of male O. rochei fits very well with its spawning season, which suggests an important function related to reproductive behavior. Observations made by Mann et al. (1997) on Ophidion marginatum corroborate this hypothesis, as they showed that this species produces long multiple-pulsed sounds before and during spawning. In their study, males started to call at dusk while they were buried in the sand or swimming over the females, and sound pro- duction ceased approximately 15 min after eggs were released by the females. As O. rochei and O. margina- tum share many biological characteristics such as simi- lar diets, external phenotypes, burrowing behaviors, sexual dimorphism in sonic apparatuses, and long, pulsed calls (see Courtenay 1971; Mann et al. 1997; Nielsen et al. 1999; K ever et al. 2012), it can be reason-
1320 Marine Ecology 37 (2016) 1315–1324 ª 2016 Blackwell Verlag GmbH Kever, Lejeune, Michel & Parmentier Ophidion rochei calling activity in Calvi Bay
Fig. 6. Daily sound production of Ophidion rochei and moon phases. Variation in daily sound production during summer 2011 is shown in black and plotted on the left y-axis. Variation in daily sound production during late spring and early summer 2013 is shown in gray and plotted on the right y-axis. Circles represent different moon phases (obtained from http://aa.usno.navy.mil/cgi-bin/). Solid white circle: full moon. Solid black circle: new moon. Circle with the right half white and the left half black: first quarter. Circle with the left half white and the right half black: last quarter. ably inferred that male calls of both of these species later in the season, sound production was concentrated are emitted in similar behavioral contexts. shortly after sunset, showing that fish most probably Here, sound production of male O. rochei started change their behavior during the spawning period. The approximately 1 h after dusk and sometimes lasted for gonado-somatic indexes of Casadevall (1991) suggest that the whole night. The highest sound production rate was spawning occurs more often in September. In the latter observed 1–3 h after sunset. A second, but smaller, peak case, the function of sound production earlier in the sea- often occurred approximately 2 h before sunrise. This is son could be different and remains to be determined. in good accordance with results obtained by Parmentier Early in the season, sounds may be used to group speci- et al. (2010b) from recordings performed in Croatia. mens as in sciaenids (Connaughton & Taylor 1995; Mann & Grothues (2009) observed a very similar pattern Lagard ere & Mariani 2006) and/or to define territories. for O. marginatum. Peaks in sound production at dusk or after sunset are very common in sciaenid species (Fish Sound production and temperature & Cummings 1972; Saucier & Baltz 1993; Mann et al. 1997; Mann & Grothues 2009) and have also been The exact moment of the annual onset of sound produc- described in other families such as Serranidae (Lobel tion cannot be clearly determined in this study, probably 1992; Sch€arer et al. 2012), Chaetodontidae (Boyle & Tri- because there are variations from year to year. Sound cas 2010), Gadidae (Brawn 1961) and Pomacentridae production started earlier and was more intense in 2013 (Parmentier et al. 2010a). In every case, sound produc- than in 2012. Male Ophidion rochei probably call during tion was mainly related to reproductive behaviors (Fish & courtship and mating behaviors and many factors have Cummings 1972; Holt et al. 1985; Lobel 1992; Saucier & been reported to affect the timing of fish reproduction: Baltz 1993; Mann et al. 1997; Boyle & Tricas 2010). photoperiod, temperature, lunar phase, rainfall, food According to Holt et al. (1985), because sciaenid species availability, habitat availability, pheromone presence and use sounds to locate mates, they are not dependent on sex ratio (Bromage et al. 2001; Takemura et al. 2004; light for spawning. These authors suggested that evening Migaud et al. 2010). Among these factors, photoperiod spawning could be advantageous because it allows for egg and temperature are the most consistent environmental dispersal at night, when zooplanktivorous fishes are less signals able to provide a reliable timing message (Migaud active. A similar hypothesis can be proposed for ophidi- et al. 2010). Photoperiod is probably the major determi- ids, as all species investigated to date produce pelagic eggs nant of the initiation and duration of the spawning sea- (Fahay 1992; Casadevall et al. 1993) and show the highest son in temperate habitats (Bromage et al. 2001; peak of sound production soon after sunset. Pankhurst & Porter 2003; Migaud et al. 2010). However, Our long-term recordings show that in O. rochei, the seawater temperature can also affect reproductive period pattern of daily sound production varied during the (Bromage et al. 2001; Pankhurst & Porter 2003; Clark reproductive period. Males first called all night long but et al. 2005; Migaud et al. 2010). Locascio & Mann (2011)
Marine Ecology 37 (2016) 1315–1324 ª 2016 Blackwell Verlag GmbH 1321 Ophidion rochei calling activity in Calvi Bay Kever, Lejeune, Michel & Parmentier even suggested that temperature could have more influ- mossambicus: male–female and male–male interactions. ence than photoperiod on the reproductive period of the Journal of Fish Biology, 62, 658–672. black drum. Our results are consistent with this hypothe- Boyle K.S., Tricas T.C. (2010) Pulse sound generation, anterior sis. Cooler temperatures can delay gonadal development, swim bladder buckling and associated muscle activity in the which may explain some differences in spawning time pyramid butterflyfish, Hemitaurichthys polylepis. Journal of 213 – (Hutchings & Myers 1994). Photoperiod is consistent Experimental Biology, , 3881 3893. from 1 year to another but temperature is not. As tem- Brantley R.K., Bass A. (1994) Alternative male spawning tactics perature was higher during late April 2013 and the first and acoustic signals in the plainfin midshipman fish, half of May 2013 compared with the same period in 2012 Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology, 96, 213–232. (dashed lines in Fig. 4), seawater temperature could be a Brawn V.M. (1961) Sound production by the cod (Gadus good candidate to explain the earlier sound production calliaras L.). Behaviour, 18, 240–255. period in 2013. Higher temperatures were recorded for Bromage N., Porter M., Randall, C. (2001) The environmental several days in May 2013 and may have promoted an ear- regulation of maturation in farmed finfish with special lier sound production onset (e.g. hormonal changes). Dif- reference to the role of photoperiod and melatonin. ferences in seawater temperature can also affect fish Aquaculture, 197,63–98. distribution (Hutchings & Myers 1994) and create spatial Casadevall M. (1991) Aspectes anat omics i biol ogics d’alguns shifts instead of temporal shifts. anguilliformes i ophidiiformes del mediterrani occidental. In 2011, the end-point of the sound production period Departament de Biologia Animal, Biologia Vegetal i was clearly at the end of September. The means for short Ecologia. Universidad autonoma de Barcelona, Barcelona: and long pulse periods of male O. rochei calls suggest that 343. temperature was higher in September 2011 than in July Casadevall M., Bonet S., Matallanas, J. (1993) Description of and August 2011. This was also the case in 2012 (Fig. 4). different stages of oogenesis in Ophidion barbatum (Pisces, Thus, the decrease in sound production during Septem- Ophidiidae). Environmental Biology of Fishes, 36, 127–133. ber 2011 was most probably not related to changes in Clark R.W., Henderson-Arzapalo A., Sullivan, C.V. (2005) temperature but more likely with the shortening of day- Disparate effects of constant and annually-cycling daylength time length. and water temperature on reproductive maturation of striped bass (Morone saxatilis). Aquaculture, 249, 497–513. Colleye O., Parmentier E. (2012) Overview on the diversity of Conclusions sounds produced by clownfishes (Pomacentridae): The main advantage of PAR compared with more classical importance of acoustic signals in their peculiar way of life. 7 – techniques to determine the reproductive period and to PLoS ONE, ,1 11. detect spawning events of nocturnal animals is its higher Connaughton M.A., Taylor M.H. (1995) Seasonal and daily cycles in sound production associated with spawning in the temporal resolution. For Ophidion rochei, it allowed us to weakfish, Cynoscion regalis. Environmental Biology of Fishes, uncover an inter-annual variation in the onset of the 42, 223–240. reproductive period. Moreover, long-term recordings Courtenay W.R. (1971) Sexual dimorphism of the sound (complete year) indicated that the pattern of daily sound producing mechanism of the striped cusk eel, Rissola production varied during the reproductive period. marginata (Pisces: Ophidiidae). Copeia, 2, 259–268. De Jong K., Bouton N., Slabbekoorn, H. (2007) Azorean rock- Acknowledgements pool blennies produce size-dependent calls in a courtship context. Animal Behaviour, 74, 1285–1292. Dr G. Lepoint (Laboratory of Oceanology, University of Fahay M.P. (1992) Development and distribution of cusk eel Li ege), Bruno Parmentier, and the staff of STARESO sta- eggs and larvae in the Middle Atlantic Bight with a tion kindly helped during field campaigns. Thanks to Dr description of Ophidion robinsi n. sp. (Teleostei: K Boyle for his insightful comments on the manuscript. Ophidiidae). Copeia, 3, 799–819. This study was supported by grants from the Fonds pour Fine M.L., Parmentier E. 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