Long-term monitoring of captive red drum Sciaenops ocellatus reveals ...

Journal of Fish Biology (2016) 88, 1776–1795 doi:10.1111/jfb.12938, available online at wileyonlinelibrary.com

Long-term monitoring of captive red drum Sciaenops ocellatus reveals that calling incidence and structure correlate with egg deposition E. W. Montie*†, C. Kehrer*, J. Yost‡, K. Brenkert‡, T. O’Donnell‡ and M. R. Denson‡ *Department of Natural Sciences, University of South Carolina Beaufort, One University Boulevard, Bluffton, SC, 29909, U.S.A. and ‡Marine Resources Research Institute, South Carolina Department of Natural Resources, P. O. Box 12559, Charleston, SC, 29422-2559, U.S.A. (Received 2 November 2015, Accepted 8 February 2016) In the present study, quantitative data were collected to clarify the relationship between calling, call structure and eggs produced in a captive population of red drum Sciaenops ocellatus. Sciaenops ocellatus were held in four tanks equipped with long-term acoustic loggers to record underwater sound throughout a simulated reproductive season. Maximal sound production of captive S. ocellatus occurred when the photoperiod shifted from 13·0 to 12·5 h of light, and the water temperature decreased to c. 25∘ C. These captive settings are similar to the amount of daylight and water temperatures observed during the autumn, which is the primary spawning period for S. ocellatus. Sciaenops ocellatus exhibited daily patterns of calling with peak sound production occurring in the evenings between 0·50 h before dark and 1·08 h after dark. Spawning occurred only on evenings in which S. ocellatus were calling, and spawning was more productive when S. ocellatus produced more calls with longer durations and more pulses. This study provides ample evidence that sound production equates to spawning in captive S. ocellatus when calls are longer than 0·8 s and contain more than seven pulses. The fact that more calling, longer calls and higher sound pressure levels are associated with spawns that are more productive indicates that acoustic metrics can provide quantitative information on spawning in the wild. © 2016 The Fisheries Society of the British Isles

Key words: passive acoustics; reproduction; Sciaenidae; soniferous fishes; sound production.

INTRODUCTION Fish sound production varies in form and function and is widespread throughout many fish families. Some of these families include catfishes (Ictaluridae, Pimelodidae, Doradidae and Mochokidae), grouper (Serranidae), haddock Melanogrammus aeglefinus (L. 1758) and cod Gadus morhua L.1758 (Gadidae), toadfishes (Batrachoididae), triglids (Triglidae), cichlids (Cichlidae), damselfishes (Pomacentridae), African freshwater fishes (Mormyyridae) and drums (Sciaenidae) (Tavolga, 1958; Fish & Mowbray, 1970; Holt et al., 1985; Fine et al., 1990; Mann & Lobel, 1995; Wilson et al., 2004; †Author to whom correspondence should be addressed. Tel.: +1 843 208 8107; email: [email protected]

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Locascio & Mann, 2005; Amorim, 2006; Gannon, 2007; Luczkovich et al., 2008; Mann & Grothues, 2009; Parmentier et al., 2009; Walters et al., 2009; Mann et al., 2010). Agonistic and courtship behaviours are the most common reasons for fish sound production. There is some debate, however, on the relationship between sound production and spawning in soniferous fish species (Luczkovich et al., 1999; Locascio et al., 2012). Fishes belonging to the Family Sciaenidae are known for their sound producing capabilities. These include species such as silver perch Bairdiella chrysoura (Lacépède 1802), spotted seatrout Cynoscion nebulosus (Cuvier 1830), black drum Pogonias cromis (L. 1766), weakfish Cynoscion regalis (Block & Schneider 1801), American star drum Stellifer lanceolatus (Holbrook 1855), Atlantic croaker Micropogonias undulatus (L. 1766) and red drum Sciaenops ocellatus (L. 1766) (Hill et al., 1987; Nieland & Wilson, 1993; Sprague et al., 2000; M. R. Collins, B. M. Callahan & W. C. Post, unpubl. data). Sciaenids are most common in turbid estuarine, coastal and bay systems. These fishes may have evolved mechanisms to produce sound to communicate more effectively in these murky environments (Holt et al., 1981; Holt, 2008). Sound production anatomy in these species involves a sonic muscle that abuts a swimbladder. This muscle contracts and vibrates near the inflated swimbladder, which produces a drumming sound. Species in the family Sciaenidae have different swimbladder and sonic muscle shapes, as well as different sonic muscle and swimbladder configurations (Ramcharitar et al., 2006; Fine & Parmentier, 2015), which create species-specific call types. In most sciaenids, only the males contain a sonic muscle and produce sound; however, both male and female M. undulatus and P. cromis contain sonic muscles and produce sound (Hill et al., 1987; Tellechea et al., 2010b). Studies that have recorded underwater sound during reproductive seasons have revealed that patterns of fish sound production coincide with patterns of reproductive condition (Connaughton & Taylor, 1995). Studies have also demonstrated an association between sound production and spawning through the simultaneous collection of acoustic recordings and eggs in the wild (Mok & Gilmore, 1983; Saucier & Baltz, 1993; Luczkovich et al., 1999; Aalbers & Drawbridge, 2008). Luczkovich et al. (1999) quantitatively compared the timing and levels of sound production in wild C. regalis with the timing and numbers of sciaenid-type eggs; these authors found a significant positive relationship. These types of comparisons are essential if scientists and managers plan to use passive acoustics as a tool to monitor fish reproduction in wild stocks. These data are challenging to obtain because it is difficult to ensure that the eggs that are collected are from the same population of fish that are producing sound (Locascio et al., 2012). The number of eggs collected in the field is probably affected by predator activity, water currents and the efficiency of plankton tows, making it an inefficient metric for estimating spawning activity. Studies using fishes held in a captive environment can control for some unaccounted variables that are present in the wild. A few studies have used this captive approach to examine the behavioural associations of sound production and spawning (Guest & Lasswell, 1978; Connaughton & Taylor, 1996; Aalbers & Drawbridge, 2008). Guest & Lasswell (1978) observed that drumming and nudging in captive S. ocellatus intensified prior to spawning. Connaughton & Taylor (1996) illustrated the association between courtship behaviour, male drumming and spawning in C. regalis held in laboratory tanks. Aalbers & Drawbridge (2008) documented call types and the association of sound production with courtship behaviour and spawning in white seabass Atractoscion

© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, 88, 1776–1795

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nobilis (Ayres 1860) maintained in a net-pen. These studies were important in providing qualitative information on the association between sound production and courtship behaviour. In the present study, the overall goal was to collect quantitative data to understand the relationship between the amount of calling and the call structure with the number of eggs collected. Wild caught S. ocellatus held in laboratory tanks were used as a model species and acoustic loggers were deployed that recorded the underwater tank environment throughout an entire, simulated reproductive season. Sciaenops ocellatus is an estuarine-dependent species ranging from Massachusetts to Key West, Florida, on the U.S. Atlantic coast and from south-west Florida to northern Mexico in the Gulf of Mexico (Lux & Mahoney, 1969). The primary spawning period occurs during mid-August through October along the Atlantic coast and the Gulf of Mexico with sexually mature adults, larvae and small S. ocellatus ( tank 2 > tank 4 > tank 3; Table II and Fig. 3). Third, photoperiod and temperature adjustments affected sound production. Generally, maximal sound production of captive S. ocellatus occurred when the photoperiod was set to 12·5L:11·5D, and the water temperature decreased to c. 25∘ C (Fig. 3). In tanks 1, 2 and 4, calling began to decrease once the temperature fell below 25∘ C in November. In tank 3, sound production of S. ocellatus was different in that calling was most prevalent during the 12·5 h light cycle and during a period when the temperature dropped from 26 to 23∘ C (i.e. from 14 to 19 November 2012) [Fig. 3(c)]. In tanks 1 and 2, abrupt drops in temperature decreased calling, while abrupt rises in temperature increased sound production (Fig. 3). Sciaenops ocellatus exhibited daily patterns of calling (Table III and Fig. 4). Generally, sound production began between 0·08 and 2·08 h before dark and continued for a period of 1·67–4·67 h, depending upon the tank and light cycle. On average, peak sound production occurred sometime between 0·50 h before dark and 1·08 h after dark (Table III). Generally, calling ended between 1·33 and 3·75 h after dark. In tank 1, peak sound production shifted to earlier times as the light cycle (i.e. sunset) changed from 1915 to 1900 to 1845 hours [Fig. 4(a)].


SPL, received sound pressure level in dB re 1 μPa.

Number of spawns Eggs collected Viable eggs collected Number of calls Number of calls between 1540 and 0000 hours Number of calls between 1540 and 0000 hours (no spawning) Number of calls between 1540 and 0000 hours (spawning) Mean calls between 1540 and 0000 hours (no spawning) Mean calls between 1540 and 0000 hours (spawning) Mean SPL from 1540 and 0000 hours (no spawning) Mean SPL from 1540 and 0000 hours (spawning) Mean call duration (s) Duration range of calls (s) Mean call duration (no spawning) (s) Mean call duration (spawning) (s) Mean number of pulses in a call Pulse range of calls Mean number pulses (no spawning) Mean number pulses (spawning)

Tank Information 61 94 604 000 89 970 000 53 329 41 801 17 403 24 398 200 ± 203 393 ± 81 120 ± 3 122 ± 1 0·70 ± 0·14 0·20 to 2·24 0·63 ± 0·16 0·78 ± 0·05 6·62 ± 2·39 2 to 25 5·43 ± 2·62 8·02 ± 0·88

Tank 1 32 55 418 000 50 270 000 20 681 20 244 8664 11 580 75 ± 132 341 ± 155 116 ± 3 121 ± 3 0·73 ± 0·17 0·19 to 2·10 0·66 ± 0·17 0·82 ± 0·12 5·89 ± 2·41 2 to 25 4·67 ± 2·01 7·48 ± 1·93

Tank 2 4 10 040 000 8 740 000 8238 3349 2366 983 17 ± 28 246 ± 151 117 ± 1 123 ± 2 0·41 ± 0·11 0·23 to 2·23 0·40 ± 0·10 0·75 ± 0·05 2·26 ± 0·65 2 to 17 2·19 ± 0·50 4·61 ± 0·79

Tank 3 33 72 710 000 61 650 000 8795 7479 820 6659 7 ± 11 202 ± 97 114 ± 1 119 ± 2 0·56 ± 0·24 0·21 to 3·53 0·43 ± 0·10 0·92 ± 0·12 3·59 ± 2·59 2 to 29 2·20 ± 0·38 7·49 ± 2·06

Tank 4

33 ± 12 58 193 000 ± 17 941 842 52 657 500 ± 16 851 149 22 761 ± 10 586 18 218 ± 8644 7313 ± 3767 10 905 ± 4992 75 ± 44 296 ± 44 117 ± 1 121 ± 1 0·60 ± 0·07 0·21 ± 0·01 to 2·52 ± 0·34 0·53 ± 0·07 0·82 ± 0·04 4·59 ± 1·01 2 ± 0 to 24 ± 2 3·62 ± 0·84 6·90 ± 0·77

Means ± s.e.

Table II. Sciaenops ocellatus call data and characteristics. Means ± s.d. reported for individual tanks and means ± s.e. of all four tanks

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Fig. 2. The relationship between received sound pressure level (SPL) and the number of calls produced by wild caught Sciaenops ocellatus held in captivity. The received SPL of the entire, 2 min wav file (i.e. the signal) was determined using automated MATLAB scripts. This calculation was completed by first applying a band pass filter to the signal (selection between 50 and 2000 Hz), then calculating the root mean square of the filtered signal and converting to a received SPL by incorporating the hydrophone sensitivity (−185 dBV μPa−1 ) and the DSG gain (i.e. 20). The relationship between the number of calls and SPL for all 2 min wav files was determined using a Pearson correlation analysis test for tanks (a) 1 (y = 0·3606x + 117·03; r2 = 0·845), (b) 2 (y = 0·48x + 114·35; r2 = 0·885), (c) 3 (y = 0·418x + 116·74; r2 = 0·365) and (d) 4 (y = 0·4203x + 114·5; r2 = 0·686).

R E L AT I O N S H I P B E T W E E N S O U N D P R O D U C T I O N A N D S PAW N I N G

Sound production played an important role in spawning of wild caught S. ocellatus held in captivity. This overall theme was supported by four major findings. First, successful spawns (i.e. eggs were present) occurred only on evenings in which S. ocellatus were calling (Fig. 5). Sciaenops ocellatus did produce sound without a corresponding spawn, but spawning never occurred without a substantial increase in calling the evening before eggs were collected. In general, autocorrelation analysis indicated that the strongest relationship between calling variables (i.e. number of calls, SPL, number of pulses in a call, and call duration) and eggs collected occurred on the same evening (i.e. lag = 0) (data not shown). Second, the likelihood that S. ocellatus spawned was significantly related to calling and SPLs [Table IV and Fig. 6(a), (b)]. According to the logistic models, the log of the odds of S. ocellatus spawning was positively related to the amount of calling and SPLs. In other words, the more calling that occurred or higher SPLs, the more likely that S. ocellatus would spawn. Third, spawning was more productive with more calling. For all tanks, more calling and higher SPLs were associated with more eggs released by females (Table V). Fourth, on evenings when


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Fig. 3. Sound production by wild caught Sciaenops ocellatus held in captivity throughout the entire study period. The number of calls in each 2 min wav file ( ) was manually counted by an observer and plotted with date with corresponding water temperatures ( ) for (a) tank 1, (b) tank 2, (c) tank 3 and (d) tank 4. (a) The numbers above the horizontal line indicate the number of hours of light present in the respective photoperiod. , an abrupt drop in temperature and a decrease in calling; , an abrupt rise in temperature and an increase in calling.

S. ocellatus did spawn, the call structure was different as compared to the structure that was observed on evenings when spawning did not occur. The likelihood that S. ocellatus spawned was significantly related to call structure [Table IV and Fig. 6(c), (d)]. According to the logistic models, the log of the odds of S. ocellatus spawning was positively related to the number of pulses in a call and call duration. In other words, if male calls contained more pulses and were longer in duration, then it was more likely that S. ocellatus would spawn [Table IV and Fig. 6(c), (d)]. In addition, spawns that were



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Table III. Hours before or after dark in which sound production occurred in captive Sciaenops ocellatus. Values represent means of all four tanks. Light cycle 1: 16 July 2012 to 5 August 2012: 14·0 h light; 1930 hours lights off. Light cycle 2: 6 August 2012 to 26 August 2012: 13·5 h light; 1915 hours lights off. Light cycle 3: 27 August 2012 to 9 September 2012: 13·0 h light; 1900 hours lights off. Light cycle 4: 10 September 2012 to 17 December 2012: 12·5 h light; 1845 lights hours off. Light cycle 5: 18 December 2012 to 25 December 2012: 11·0 h light; 1800 hours lights off Sound Production Start time Peak time End time Total time calling (h)

Light cycle 1

Light cycle 2

Light cycle 3

Light cycle 4

Light cycle 5

ndp ndp ndp ndp

−0·25 +1·08 +3·75 4

−1·33 −0·50 +1·33 2·67

−1·30 +0·47 +2·70 4

ndp ndp ndp ndp

−, hours before dark; +, hours after dark; ndp, no daily pattern observed.

more productive were associated with calls that were longer in duration and contained more pulses (Table V). DISCUSSION A C O U S T I C C H A R A C T E R I Z AT I O N O F S. O C E L L A T U S C A L L S

Sciaenops ocellatus calls were similar to the calls observed in other research studies (Guest & Lasswell, 1978; Lowerre-Barbieri et al., 2008; Parmentier et al., 2014). Lowerre-Barbieri et al. (2008) found that S. ocellatus calling occurred within a frequency range of 100–1200 Hz, while Guest & Lasswell (1978) reported that S. ocellatus pulses contained sound energy up to 2500 Hz with dominant energy in the 240–1000 Hz range. Parmentier et al. (2014) found that captive S. ocellatus produced calls that contained three or four pulses, and the dominant frequency ranged from 78 to 157 Hz. In the present study, variation in S. ocellatus call structure (i.e. number of pulses and call duration) was observed within a tank. Studies have demonstrated that differences in fish size can influence pulse duration and dominant frequencies. For example, in C. regalis, as fish increase in size, the frequency range of calling decreases and the sound pressure level and pulse duration increase (Connaughton et al., 2000). In whitemouth croaker Micropogonias furnieri (Desmarest 1823), dominant frequency and interpulse interval decrease, while pulse duration increases with fish size (Tellechea et al., 2010a). In the present study, male S. ocellatus were of similar size, and variation in call structure was most likely attributed to whether or not spawning occurred. This observation is discussed further in the section below that focuses on how sound production influences spawning success. For each 2 min wav file obtained, the broadband received SPL of that entire recording was calculated. The number of calls counted in the 2 min wav files correlated positively with the mean received SPL (see Fig. 2). Mean SPL is a function of the number of calls, the number of pulses in a call, the sound intensity of each call and the distance of the sound source from the recorder. The relationship between calling and received SPL is important because SPL is often the more useful metric in quantifying sound production


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Time (hours) Fig. 4. Daily patterns of calling by wild caught Sciaenops ocellatus held in captivity. To examine these patterns, the mean ± s.d. number of calls was determined for each time interval (e.g. 1200–1202, 1220–1222, 1240–1242, 1300–1302 hours, etc.) during each photoperiod (i.e. 14 h of light with lights turning off at 1930 hours; 13·5 h of light with lights turning off at 1915 hours; 13·0 h of light with lights turning off at 1900 hours; 12·5 h light with lights turning off at 1845 hours and 11·0 h of light with lights turning off at 1800 hours) ( , 1915 hours lights off; , 1900 hours lights off; , 1845 hours lights off).

in the wild, where it can be challenging to count overlapping calls of a spawning aggregation. In addition, long-term monitoring of spawning sites using autonomous acoustic recorders can generate thousands of acoustic files. Having a MATLAB code determine the mean received SPL of each acoustic file as a means to quantify sound production is much less time intensive than having an observer manually count calls. The one drawback in calculating received SPL is that the level depends on the distance from the spawning aggregation, which is typically unknown in sciaenid recordings. L I G H T C Y C L E A N D T E M P E R AT U R E A F F E C T S S O U N D P RO D U C T I O N

Maximal sound production of captive S. ocellatus occurred when the photoperiod shifted from 13·0 to 12·5 h of light, and the water temperature decreased to c. 25∘ C. These captive settings are similar to the amount of daylight and water temperatures observed during the autumn, which is the primary spawning period for


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Fig. 5. Sound production and spawning of wild caught Sciaenops ocellatus held in captivity throughout the entire study period. Calls per day ( ) and the number of eggs (i.e. the next morning; ) were plotted with the date for tanks (a) 1, (b) 2, (c) 3 and (d) 4.

S. ocellatus (Murphy & Taylor, 1990; Ross et al., 1995; Luczkovich et al., 2008). In the south-eastern U.S.A., sound production of S. ocellatus has been detected from August to mid-October (Lowerre-Barbieri et al., 2008; M. R. Collins, B. M. Callahan & W. C. Post, unpubl. data). This seasonal shift in calling frequency is due to changes in testosterone levels, which affects the output of the central nervous system and sonic muscle mass. For example, in C. regalis, the sonic muscle triples in mass as the spawning season approaches (Connaughton & Taylor, 1994). This hypertrophy is driven by elevated androgen levels, which are triggered by photoperiod and temperature cues that initiate sexual recrudescence (Connaughton & Taylor, 1994). Sonic muscle hypertrophy also coincides with seasonal patterns of sound production, with


Predictor variable

Number of calls Mean SPL (dB re 1 𝜇Pa) Number of pulses Call duration (s)




Tank

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Logit(y) = −7·294 + 0·127x Logit(y) = −261·428 + 2·243x Logit(y) = −13·532 + 3·558x Logit(y) = −26·058 + 37·672x




Logistic model

2·913 4·971 2·994 2·447

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6·019 5·835 4·498 3·819

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z 1·007 1·692 0·694 5 511 251·887 1·010 1·509 1·878 1814·287 1·035 4·824 6·510 3 056 491·054 1·135 9·425 0·003 2·295E + 016