Vocal behavior of the endangered splendid toadfish and potential masking by anthropogenic noise

Vessel‐related noise is a potential stressor for coral reef fauna. The Parque Nacional Arrecifes de Cozumel (PNAC) is a Mexican Marine Protected Area that is exposed to pervasive vessel traffic. PNAC is also the primary range of splendid toadfish (Sanopus splendidus, family Batrachoididae), an IUCN red‐listed soniferous fish for which vessel noise may represent a threat. We conducted a passive acoustic monitoring survey during summer of 2017 at Paraiso Reef in PNAC and obtained the first scientific recordings from splendid toadfish, enabling a vocal characterization of the species. We simultaneously collected data on sound levels of vessels passing near the reef. High noise levels of cruise ship and small motorboat traffic caused elevated anthropogenic sound pressure levels for up to 15 hr per day in the same bandwidth as toadfish vocalizations. A single cruise ship added up to 4 dB above nighttime ambient levels while small motorboat traffic added up to 7 dB. The overlap of toadfish vocalizations and vessel‐related noise highlights the susceptibility of splendid toadfish to acoustic masking and reduction in communication space throughout the day, warranting further study. Because acoustic communication is critical to toadfish reproductive success, noise from cruise ships and small motorboats may threaten splendid toadfish individuals or population viability.

While the principle concerns of anthropogenic noise impacts to fishes include altered perception and production of sounds (Popper & Hawkins, 2019), such as masking (Putland, Merchant, Farcas, & Radford, 2018;Vasconcelos, Amorim, & Ladich, 2007), an emerging body of the literature has recently demonstrated responses to noise outside of direct auditory or communicative contexts, including developmental changes (Fakan & McCormick, 2019), increased stress, altered foraging (Magnhagen, Johansson, & Sigray, 2017), disrupted schooling (Sarà et al., 2007), and increased susceptibility to predation (Simpson et al., 2016;Simpson, Purser, & Radford, 2015). The diversity of possible vessel noise effects on fishes suggests that more urgent study is needed to understand the consequences of high vessel traffic on coral reefs and their associated fauna.

| Monitoring the health of Cozumel's coral reefs
Recent years have seen an increase in the number of cruise ships visiting Cozumel island, particularly after the completion of a third cruise ship terminal in 2015, which made Cozumel the second busiest cruise port in the world (Caribbean Journal staff, 2014;Mexico News Daily, 2019;OECD, 2017). In the 2017/2018 cruise year, Cozumel received over a thousand cruise ships with an estimated 4.1 million passengers, and up to eight ships per day, an increase of approximately 40% from 2014 to 2015 (Business Research and Economic Advisors, 2018;CONANP, 2016; Port Administration of Quintana Roo APIQROO, 2017; Secretaría de Medio Ambiente y Recursos Naturales, Secretaría de Turismo, 2015). Data related to dive tourism are more difficult to find and quantify, but internet searches resulted in the identification of hundreds of companies offering SCUBA dive trips in Cozumel. In September 2019 there were 243 boats, each carrying a maximum number of 60 passengers, with permits from the National Commission of Natural Protected Areas Mexico (CONANP) to enter the Cozumel Reefs National Park (Parque Nacional Arrecifes de Cozumel [PNAC]) (CONANP and SEMARNAT, 2019). Cozumel reefs have already suffered from intense fishing activities and are under increasing pressure from this tourism. In just 27 years  live coral cover off Cozumel declined by 13% due to impacts from tourists, small motorboat pollution, and other anthropogenic threats compared to an average coral cover decrease of 11% on the Mesoamerican Barrier Reef (Jackson, Donovan, Cramer, & Lam, 2014;Wilkinson, 2008;Wilkinson & Souter, 2008). Regular baseline monitoring of the health of Cozumel's extensive reefs is currently led by locally based CONANP staff. Since 2004, scientists have conducted monthly physicochemical monitoring at 11 reef sites and traditional photo-transect monitoring every 6 months at six reef locations to measure the percentage of coral cover and to count and photo identify fish and benthic species present at each site (CONANP, 2020;Garcia Salgado et al., 2008;Gress, Arroyo-Gerez, Wright, & Andradi-Brown, 2018). Additional site-specific photogrammetry studies documenting coral assemblages were conducted in 2018 in PNAC (Hernández-Landa, Barrera-Falcon, & Rioja-Nieto, 2020). These types of surveys are time and labor intensive, limited to depths accessible to human divers, and rarely conducted at night. Diver surveys focused on marine fauna frequently overlook cryptic or nocturnally active species such as toadfish, and species that may be correlated with reef health such as snapping shrimp (Sale, 1997;Willis, 2001). Diver surveys can also introduce sampling error and bias associated with behavioral responses of marine fauna to human presence (Pais & Cabral, 2018). While providing a basic understanding of reef health, visual surveys do not account for all potential impact producing factors, specifically noise, on marine fauna.

| Study objectives and focal species
Prior to this study, no PAM had been conducted within PNAC. Initially, the research team was focused on obtaining the first scientific recording of vocalizations from one of the most iconic Cozumel reef species, the splendid toadfish (Sanopus splendidus, Family Batrachoididae) (Figure 1). Consultation with CONANP suggested that local conservation managers were concerned about the potential effect of cruise ship noise on reef fishes, including S. splendidus. To address this concern, the study objectives were expanded to include an analysis of cruise ship and small motorboat noise to determine if there were potential effects of the anthropogenic noise levels on S. splendidus. Autonomous acoustic recorder data were processed and analyzed to identify noise sources and determine the frequency overlap of vessel noise and S. splendidus vocalizations. Based on that information, CONANP staff could assess the risk that increasing vessel noise may pose to S. splendidus. This work may be more broadly extrapolated to other vulnerable or data deficient species that communicate in the same frequency band.
S. splendidus was originally described as an endemic species to Cozumel (Collette, 1974), and is currently categorized as an endangered species by the International Union for the Conservation of Nature (IUCN) (Collette, Aiken, & Polanco Fernandez, 2015). The splendid toadfish's endangered status is based on an estimated area of occupancy that is less than 500 km 2 (IUCN estimates it as~109 km 2 ) and is severely fragmented or limited to less than five geographic locations within that area (Collette et al., 2015). The habitat fragmentation is assumed to result in increased extinction risks to the taxon since most of its individuals are found in small and relatively isolated subpopulations. In addition, the ranking also assumes the population's continuing decline, poor habitat quality, and loss of mature, reproducing individuals (Collette et al., 2015;Hawkins, Roberts, & Clark, 2000; IUCN Standards and Petitions Committee, 2019).
A recent analysis of recreational diver records suggests that the splendid toadfish population may have a broader distribution than described by IUCN, with observations as far north as Isla Mujeres, Mexico and as far south as the Sapodilla Cayes, Belize, a distance of nearly 600 km (Moreno Mendoza & Barrientos Medina, 2019). The species' full habitat range and the connectedness of this range remain unknown. A lack of information on the species' population size, distribution and trends, baseline life history or ecological data leads to uncertainty in the conservation status.

| Survey location and design
The study area was located on Paraiso Reef in PNAC. S. splendidus have officially been observed at 24 sites on the leeward site of Cozumel (Moreno Mendoza & Barrientos Medina, 2019), but they are reliably sighted at Paraiso Reef so there was a high likelihood of species presence for acoustic recordings. Indeed, multiple den sites were visually observed with vocalizing occupants during both pre-deployment surveys and during the equipment deployment and retrieval. This site was also chosen in consultation with CONANP staff because it is the closest dive site (<400 m) to the Puerta Maya Pier cruise ship terminal on Cozumel ( Figure 2). Cruise ships following a transit corridor into the terminal must pass within a few hundred meters of Paraiso Reef, and it was hypothesized that sound pressure levels (SPLs) from the cruise ships might be negatively affecting marine fauna.
In addition to cruise ships transiting in and out of Puerta Maya within 300-400 m of the study site, nearly all dive boats pass directly over Paraiso Reef enroute to other dive sites. It is also frequented by large groups of cruise ship snorkelers and beginner SCUBA divers because of its ease of access, shallow water depths (maximum 17 m) and proximity to shore (~180 m). Submarine excursions visit the southern end of the reef up to three times daily. It is also one of the reef sites most frequented by night divers. This combination of human use results in high intensity and extended exposures of Paraiso Reef fauna to vessel noise, light, and people, relative to other reef locations on the island.

| Data collection
JASCO Applied Sciences (JASCO) and CONANP scientific divers deployed an Autonomous Multichannel Acoustic Recorder Generation 3 (AMAR-G3) with four M36-V35-100 omnidirectional hydrophones (Geospectrum Technologies Inc., −165 ± 3 dB re 1 V/μPa sensitivity) set 1 m above the sea floor and protected by hydrophone cages. The cages were covered with shrouds to minimize noise artifacts from water flow. The AMAR was placed in a sandy site in 11 m water depth (20.472568 N, 86.98093 W) among sparsely distributed coral outcrops and rocky overhangs that provided habitat for several S. splendidus dens (Figures 3 and 4). Prior to the placement of hydrophones, divers visually confirmed at least three occupied den locations within <10 m from the AMAR to ensure that recorded vocalizations could be attributed to the splendid toadfish. The AMAR operated on a duty cycle alternating between 14 min at 32,000 Hz and 60 s at 375,000 Hz. The intermittent high-frequency sampling at 375,000 Hz was performed to capture marine mammal vocalizations, if present, but none were acoustically detected. The recordings occurred continuously over 50-days from July 14 to September 3, 2017.

| Toadfish vocalization detections
Though there are many toadfish species with specific acoustic differences within the family, toadfish advertisement sounds are typically about 0.5-1 s in duration, have a fundamental frequency (ƒ 0 ) between 75 and 300 Hz, and have rich harmonic content. A previous study of the closely related Sanopus astrifer (Mosharo & Lobel, 2012) showed that vocalizations from this genus are frequency modulated with an increase in frequency over the call. The general properties of the related S. astrifer vocalization (Mosharo & Lobel, 2012) were used to infer the presence of toadfishes at the study site. While S. astrifer does not occur in Cozumel (Collette, 2002), there are two sympatric species of Sanopus documented in Cozumel, S. splendidus and S. johnsoni (Collette, 1974); neither of which has previously been recorded. S. splendidus specimens have been collected from around the island and surrounding area (Collette, 1974;Collette, 2002;Moreno Mendoza & Barrientos Medina, 2019), while S. johnsoni is only known from the location where it was discovered at the southern end of Cozumel at Palancar Reef (Collette, 1974).
Using 12, high signal to noise ratio (SNR) putative toadfish calls manually identified in the recordings, a template-based detection algorithm was trained in Raven 2.0 Sound Analysis Software (Bioacoustics Research Program, 2017). The template detector was used to identify the temporal occurrence of toadfish calls on hydrophones 2 and 4. Hydrophones 1 and 3 were deployed for redundancy and had overlapping detection ranges with hydrophones 2 and 4, respectively, and contain the same detections.
Recall of the detector (TP/TP + FN) was 71.4% and Precision (TP/TP + FP) was 33.3%, where TP = true positive detections, FN = false negative detections, FP = false positive detections. Hours with no true positive F I G U R E 3 Schematic of the deployment configuration, showing placement of the AMAR relative to patch reefs and hydrophones (indicated by numbers in blue circles) F I G U R E 4 (left) AMAR and (right) hydrophones deployed 1 m above the sea floor in 11 m water depth in a sandy site adjacent to three toadfish dens detections were manually reviewed to identify false negative detections. All detection events were visually reviewed to discard false positive detections, and false negative events were included with true positives in call occurrence analyses.
The spectral and temporal properties of toadfish calls were determined using Raven 2.0 processing discrete Fourier transform on 8,192 samples and a Hann window with 75% overlap, yielding a 3.91 Hz, 0.016 s resolution.

| Ambient sound levels and time series analysis
Ambient sound analysis provides a quantitative description of the underwater soundscape and changes over time. Data were analyzed for ambient sound levels and included an estimation of the contribution of vessel sound energy to the total measured soundscape. The results were combined and presented in five ways: (1) spectrogram for the entire deployment duration ( Figure  7); (2) exceedance percentiles of the decidecade-band SPL (ISO 18,405) (top Figure 8); (3) exceedance of the limits of prevailing noise (Wenz, 1962) percentiles of the PSD levels (bottom Figure 8); (4) minute SPL 1-min for various frequency bands as functions of time (Figure 9), and (5) daily SPL 24h computed for the total received sound pressure ( Figure 11).
Ambient sound level spectrograms were created using the JASCO software PAMLab, an acoustic inspection tool software program, a Hamming-windowed fast Fourier transform (FFT) with 1 Hz resolution and 50% window overlap. The 32,768-point FFT performed with these settings were averaged to yield 1 min averaged spectra. The 50th percentile (median of 1 min spectral averages) were compared to the Wenz ambient noise curves (Wenz, 1962), which show the variability of ambient spectral levels off the U.S. Pacific coast as a function of frequency for a range of weather, vessel traffic, and geologic conditions. 3 | RESULTS

| Toadfish vocalizations characterization
An initial visual inspection of spectrograms of the audio data immediately revealed a variety of biological sounds, including harmonic, frequency modulated signals closely resembling previously described toadfish vocalizations ( Figure 5). Unfortunately, most biological sounds recorded on Paraiso Reef could not be identified to a species level. We used two lines of evidence to support the hypothesis for the identity of the putative S. splendidus calls: (1) we assumed that these calls would have similar acoustic properties of other toadfish calls (duration, frequency, modulation), and (2) hydrophones were deliberately placed adjacent to visually confirmed S. splendidus dens, and therefore it was predicted that the calls with the highest received levels were produced by S. splendidus and not by other toadfish species.
F I G U R E 5 Representative focal Sanopus splendidus calls with many short duration (~1 s) harmonic sounds and ƒ 0 = 75 Hz. Panels (a), (c), (e), (g) show a filtered waveform of the signal (bandpass filtered 0-1,000 Hz), and panels (b), (d), (f), (h) show the corresponding spectrograms (spectrogram settings: Hann window, dFT = 8,192, 75% overlap, 3.61 Hz and 0.64 s resolution). Both amplitude and power are shown as calibrated received levels based on the known sensitivity of the AMAR Recorded vocalizations were frequency modulated with a slightly concaved frequency contour, a mean (±SE) 0.82 ± 0.03 s duration, and a frequency increase of 90.9 ± 8.9 Hz ( Figure 5). The initial call was occasionally followed by 1-3 shorter notes with the same frequency but different frequency contours ( Figure 5).
Toadfish vocalizations were detected across multiple hours every day of the survey from July 14 to September 3, 2017 on hydrophones 2 and 4, with a significant increase at night ( Figure 6, Table 1). Even though there were no obvious habitat differences between the hydrophone positions, there were more S. sanopus calls detected on hydrophone 2 than hydrophone 4 (Figure 6(a)).

| Ambient and anthropogenic sound levels
The broadband hourly SPL 1h averaged over the 50-day recording period was 120 dB re 1 μPa. The data showed a clear and repeated daily pattern of human activity beginning with the arrival of cruise ships at dawn and ending with recreational dives on the reef after dusk. Long-term spectral averages along with median band-level series provide an overview of frequency over time in the soundscape. Over the 50-day recording period, broadband vessel sounds dominate the soundscape. The full study period spectrogram showed a continuous and repetitive pattern of higher SPLs during daylight and lower sound levels during nighttime, with small motorboat noise being the main contributor to the local soundscape during daylight (Figure 7).
Interesting features of the soundscape during the study period included tropical storm Franklin, which was a clearly detected event on August 8; sound level peaks from the daily cruise ship arrivals and departures; and in at least one instance, an active acoustic echosounder operating the entire time a cruise ship was at port (Martin, Morris, Bröker, & O'Neill, 2019).
Sound level statistics quantify the observed distribution of recorded sound levels (e.g., Wenz, 1962) (Figure 8). The different percentile levels (L 5 , L 25 , L 50 , etc.) are the sound level exceeded by n% of the data. L max is the maximum recorded sound level. L mean is the linear arithmetic mean of the sound power. Decidecade-band distribution (Figure 8(a)) and PSD (Figure 8(b)) plots were directly compared to a Wenz plot (Wenz, 1962), providing a detailed spectral distribution. Vessel noise was the primary sound source that exceeded the limits of prevailing noise in the PSD L mean percentile with frequency band of 40-1,000 Hz (Figure 8(b)). Cruise ships increased sound levels the most in the 40-100 Hz band, while small motorboats increased sound levels in the 100-1,000 Hz band (Figure 8(b)). The increase of all percentiles above 1,000 Hz was likely due to reef biological sounds (Figure 8 (b)).

| Vessel noise in the soundscape
The ambient soundscape included anthropogenic sound from cruise ships and small motorboats ferrying tourists and recreational divers to and over Paraiso Reef. On a typical busy-day (Table 2) several anthropogenic sound sources were detected. Figure 9 shows the recorded median minute SPL 1-min including all vessel (cruise ships and small motorboats) sounds that were broadband (20-10,000 Hz) with low-frequency components (blue [10-100 Hz] and red [100-1,000 Hz] lines) that overlap with fish vocalization frequencies (75-300 Hz). The peaks (exceeding 120 dB SPL 1-F I G U R E 6 (a) Daily and (b)  F I G U R E 8 (a) Exceedance percentiles and mean of decidecade SPL 1-min averaged over the 50-day recording period and (b) exceedance percentiles and probability density (greyscale) of 1-min PSD levels compared to the limits of prevailing noise (Wenz, 1962) min ) within 1,000-16,000 Hz (green lines) at approximately dawn (between 07:00 and 10:00 a.m. local time) and dusk (between 6:00 and 7:00 p.m. local time) represent the arrival and departure of cruise ships passing within 400 m of Paraiso Reef as they transit to and from the Puerta Maya and SSA Mexico cruise ship terminals. High sound levels were also commonly observed between 2:00 and 3:00 p.m. that was attributed to returning small motorboats to the nearby marina and other diver disembarkment points. The peak within 10-1,000 Hz (red and blue lines) at 8:00 p.m. local time is associated with the small motorboats arriving at Paraiso Reef for night dives. The relatively flat recording line (green and yellow) at medium and high frequencies (above 1,000 Hz) during the night is presumed to be crustaceans, primarily snapping shrimp. Sounds in the 10-100 Hz band include biological activity on the reef (blue), including toadfish vocalizations.
The arrival and departure of cruise ships at Puerta Maya and the SSA Mexico terminals is a significant contributor to the Paraiso Reef soundscape. Figure 10 shows the number of cruise ship Port-of-Cozumel calls during the study period. The number above each bar indicates the number of cruise ships present each day at Puerta Maya and SSA Mexico terminals closest to Paraiso Reef. There were no cruise ship port calls to Cozumel on Sundays. While the typical busy-day (July 28) used in sound level comparisons included the arrival and departure of three cruise ships, it is important to note that there are many days throughout the year when cruise ship numbers are higher.
On August 8, Tropical storm Franklin passed over Cozumel island. This event was clearly recorded in the acoustic data. The Carnival Breeze cruise ship was diverted to a different port of call that day, reducing the cruise ship arrivals at Puerto Maya to one and Cozumel ports were closed to all small motorboats. This natural event significantly decreased the daily SPL 24h on this day ( Figure 11). This natural event provided an unexpected opportunity to compare the daily sound levels between a "busy" activity day with significant small motorboat traffic and three cruise ships passing near the AMAR (July 28); the day during tropical storm Franklin ("storm" day), where small motorboat traffic was limited, but one cruise ship made its usual port of call (August 8); and a "Sunday" activity day (August 20) with no cruise ships, but typical small motorboat traffic ( Figure 12). This is in comparison to the measured soundscape levels at "night" (after dusk and before dawn) without anthropogenic sound inputs, which registered a SPL 9h of 112 dB ( Table 2).
The comparison of these days that reflect varying anthropogenic activity levels suggests that on average, the arrival of one single cruise ship to the pier nearest Paraiso Reef adds up to 4 dB (1.6 times) to the ambient soundscape levels during the daylight hours. The small motorboat traffic without cruise ship arrivals on Sunday can add up to 7 dB (2.2 times). The arrival of several cruise ships (three or more) together with the presence of small motorboat traffic around the study area adds up to T A B L E 2 Comparison of sound pressure levels for different scenarios: "busy," "Sunday," "storm," and "night." The ΔSPL (dB) column represents the absolute difference between the sound pressure level (SPL) (dB re 1 μPa) at "night" and those scenarios measured during daylight Without any anthropogenic noise F I G U R E 9 Median minute SPL 1-min measurements for various frequency bands for the Paraiso Reef data. By taking the median value across all days, the sound of the cruise ship arrival / departures and evening dive boat activity are easy to identify. The continuous activity of crustaceans elevates the sound levels above 1,000 Hz throughout the day and night 12 dB (four times). It is thus apparent that both cruise ships and small motorboats are meaningful contributors to the soundscape, but that small motorboats are the largest contributor of anthropogenic noise to the soundscape because of the duration of the activity, which averaged approximately 15 hr per day, relative to ephemeral cruise ship arrivals and departures (Table 2).

| DISCUSSION
The Cozumel Paraiso Reef study focused on the splendid toadfish, demonstrated the value of PAM survey data as a tool for understanding vulnerable species and habitats that may lead to conservation initiatives. We present the first description of acoustic recordings of S. splendidus vocalizations that can be effectively used by scientists and managers to determine the species' occurrence, habitat range, and behavior and ecology, including mating and spawning (sensu Bertucci, Lejeune, Payrot, & Parmentier, 2015;Caiger et al., 2020;Luczkovich, Pullinger, Johnson, & Sprague, 2008;Wall et al., 2014). Recent quantitative approaches allow for estimating population density and abundance based on calling patterns (Marques et al., 2013), and these approaches could also be applied to S. splendidus.
In addition to S. splendidus, there are other toadfish found in Cozumel; S. johnsoni was also described as a Cozumel endemic (Collette, 1974). This species is less colorful than the S. splendidus and is highly cryptic with limited field observations. Few specimens have been deposited in museum collections, and it is considered data deficient by the IUCN. Opsanus dichrostomous and S. reticulatus have also been collected on the Yucatán Peninsula (Collette, 1974(Collette, , 2001Collette, 2002). Only S. splendidus was observed during deployment and hydrophones were placed near occupied toadfish dens. Therefore, it is most likely that the focal, high SNR toadfish sounds recorded belonged to our targeted species, S. splendidus. Given the similar characteristics of all toadfish vocalizations, information from this initial survey can be used in future efforts to improve management and conservation outcomes for other toadfish species and Caribbean coral reefs in general.

| Potential impacts of noise exposure on S. splendidus
There is a lack of quantitative information on the impacts of anthropogenic noise on fishes, turtles and other reef fauna, but preliminary recommendations for acoustic thresholds for these species suggest that sound levels must be quite high to cause injury (Popper et al., 2014). The swim bladder of toadfish is not thought to be involved in their hearing (Bass, Bodnar, & Marchaterre, 1999;Coffin et al., 2014;Fay & Simmons, 1999) so toadfish are not as susceptible to noise-induced hearing loss as fish whose swim bladder transmits sound pressure to the ears (Popper et al., 2014). While hearing damage is not expected at the noise levels recorded in this study (see Popper et al., 2014), fish do listen for changes in background sounds to detect approaching predators, to find prey, and to locate mates for breeding (Ladich, (McKibben & Bass, 1998;Zeddies, Fay, Alderks, Acob, & Sisneros, 2010). Thus, it is highly likely that acoustic communication plays an important role in the social and reproductive behaviors of S. splendidus and masking of advertisement vocalizations by vessel noise could impair the reproductive success of these batrachoidids.
This study found that the soundscape of Paraiso Reef during daylight is mainly comprised of anthropogenic sounds from vessel activity. The recorded vessel noise in this study is in the frequency bands (50-500 Hz) that overlap in frequency with previously described toadfish vocalizations (Vasconcelos et al., 2007) and those collected in this study.
Sound levels recorded at the study location were 4-12 dB (1.6-4 times) higher during daylight when both cruise ships and small motorboats were active versus nighttime when there was little or no human activity except for night dive boats. Daylight peak traffic times were 07:00-10:00 a.m., 2:00-3:00 p.m., and 6:00-7:00 p. m., with SPL 1-min exceeding 120 dB for several minutes. Sound level measurements from the activity of only small motorboats near Paraiso Reef increase noise levels by at least 4-7 dB above ambient for sustained periods of time. Vessel noise levels recorded were broadband (20-10,000 Hz) with a percentile L mean exceeding the limits of the Wenz ambient noise curves from 40 to 1,000 Hz.
The study results suggest that the anthropogenic noise produced by small motorboats starting at dawn and extending into the nighttime, is equivalent to, or possibly more impactful than that produced by cruise ships, particularly from a temporal perspective. This is similar to findings in other studies (Picciulin, Codarin, & Spoto, 2008;Scholik & Yan, 2002). The pervasive occurrence of vessel noise increases acoustic masking of advertising toadfish and decreases the area over which fish can acoustically communicate (Putland et al., 2018) in this study for 12-15 hr of the day. The diel nature of the species' vocalization may mitigate the effects of masking to some extent, but the impact of this extended period of masking on individuals and the population is unknown.
In addition to communication masking, other possible behavioral effects that could result from the SPLs recorded at the study site include greater depredation Simpson et al., 2016) and increased levels of cortisol (stress hormone) leading to immunosuppression. The cumulative effect of these kinds of behavioral disturbance could have population consequences, particularly when combined with other reef stressors.
Examples of management and noise mitigation that could be implemented to reduce potential impacts in the Cozumel tourist zone include the creation of exclusion zones for certain types of boats; offering financial incentives such as lower harbor fees to quieter ships and small motorboats; and establishing navigation routes that direct transiting vessels outside the reef areas. Vessel speed reductions have been shown to decrease vessel noise, with 10%-15% speed reductions equating to 1 dB attenuation (Wladichuk, Hannay, MacGillivray, Li, & Thornton, 2019). Designating slow speed zones for small motorboats may be required to alleviate noise pollution in already degraded habitats. Ocean users and resource managers are required to work cooperatively to design policy that leads to success by developing achievable and enforceable measures to avoid, minimize and mitigate the possible significant adverse impacts of anthropogenic underwater noise.
To increase the understanding of healthy versus degraded reef soundscapes and potential impact of anthropogenic noise, it is necessary to continue monitoring other barrier reef locations at different times of the year. Additional research is also needed to better understand the habitat distribution, abundance, and possible threats to species communications, which is essential to reproduction and dispersion. Future deployments along the Mesoamerican Barrier Reef would provide insight into the answers to these questions.