Listening forward: approaching marine biodiversity assessments using acoustic methods

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Mooney, T. A., Di Iorio, L., Lammers, M., Lin, T., Nedelec, S. L., Parsons, M., Radford, C., Urban, E., & Stanley, J. Listening forward: approaching marine biodiversity assessments using acoustic methods. Royal Society Open Science, 7(8), (2020): 201287, doi:10.1098/rsos.201287.Ecosystems and the communities they support are changing at alarmingly rapid rates. Tracking species diversity is vital to managing these stressed habitats. Yet, quantifying and monitoring biodiversity is often challenging, especially in ocean habitats. Given that many animals make sounds, these cues travel efficiently under water, and emerging technologies are increasingly cost-effective, passive acoustics (a long-standing ocean observation method) is now a potential means of quantifying and monitoring marine biodiversity. Properly applying acoustics for biodiversity assessments is vital. Our goal here is to provide a timely consideration of emerging methods using passive acoustics to measure marine biodiversity. We provide a summary of the brief history of using passive acoustics to assess marine biodiversity and community structure, a critical assessment of the challenges faced, and outline recommended practices and considerations for acoustic biodiversity measurements. We focused on temperate and tropical seas, where much of the acoustic biodiversity work has been conducted. Overall, we suggest a cautious approach to applying current acoustic indices to assess marine biodiversity. Key needs are preliminary data and sampling sufficiently to capture the patterns and variability of a habitat. Yet with new analytical tools including source separation and supervised machine learning, there is substantial promise in marine acoustic diversity assessment methods.Funding for development of this article was provided by the collaboration of the Urban Coast Institute (Monmouth University, NJ, USA), the Program for the Human Environment (The Rockefeller University, New York, USA) and the Scientific Committee on Oceanic Research. Partial support was provided to T.A.M. from the National Science Foundation grant OCE-1536782

Passive acoustic monitoring for assessment of natural and anthropogenic sound sources in the marine environment using automatic recognition

In the marine environment, sound can be an efficient source of information. Indeed, several marine species, including fish, use sound to navigate, select habitats, detect predators and prey, and to attract mates. Therefore, all the abiotic, biotic and manmade sounds that comprise the soundscape, have the potential to be used to assess and monitor species and marine environments. Passive acoustic monitoring (PAM) involves the use of acoustic sensors to record sound in the environment, from which relevant ecological information can be inferred. This thesis studied marine soundscapes, with special attention on fish communities, anthropogenic noise, and applied several methods to analyse acoustic recordings. Most of the focus was on the Tagus estuary, where the presence of two highly vocal species is known: the Lusitanian toadfish (Halobatrachus didactylus) and the meagre (Argyrosomus regius). Azorean and Mozambique soundscapes were also analysed. Several methods were applied to extract information and to visualize soundscape characteristics, including sound recognition systems based on hidden Markov models to recognize fish sounds and boat passages. Analysis of several types of marine environments and time scales showed several advantages and disadvantages of different methods. The use of sound pressure level on different frequency bands allowed the quantification of daily and seasonal patterns. Ecoacoustic indices appear to be cost-effective tools to monitor biodiversity in some marine environments. Using automatic recognition, vocal rhythms (diel and seasonal patterns) and vocal interactions among individuals were also characterized. Furthermore, boat noise effects on fish were studied: we encountered impacts on the audition, vocal behaviour and reproduction. Overall, we used PAM as a tool to remotely assess and monitor soundscapes, biodiversity, fish communities’ seasonal patterns, fish behaviour, species presence, and the effect of anthropogenic noise aiming to contribute for the management and conservation of marine ecosystems

Characterization of Soundscapes in Shallow Water Habitats of the Florida Keys (USA) and Their Influence on the Settlement of Larval Fish and Invertebrates

In recent decades, changes in climate and water quality in Florida Bay and the Florida Keys (FL, USA) caused expansive cyanobacteria blooms that in turn precipitated massive sponge die-offs that drastically altered sponge-dominated hard-bottom communities in south-central Florida Bay. This area served as a model system to explore the effect of ecosystem change and habitat restoration on underwater soundscapes and larval recruitment. I had four main objectives: (1) characterize the underwater soundscapes of three near-shore, benthic habitats: mangrove islands, seagrass meadows, and hard-bottom (Chapter 2); (2) quantify larval settlement within healthy, degraded, and restored hard-bottom areas to test whether habitat degradation altered larval settlement (Chapter 3); (3) empirically test the role of sound in promoting larval recruitment to hard-bottom habitat (Chapter 3); and (4) employ the passive sonar equation and distance sampling techniques to evaluate how the loss of large sponges affected the densities and abundances of snapping shrimp (Chapter 4). I found that near-shore habitats exhibit distinct soundscapes, that habitat degradation alters those soundscapes, and that habitat restoration can reestablish natural soundscapes. Habitat type and time of day significantly affected soundscapes, whereas lunar phase did not. Healthy hard-bottom and mangrove habitats exhibited louder spectra and more snapping shrimp snaps than did degraded hard-bottom or seagrass beds. However, four years after restoration, the acoustic spectra and numbers of snapping shrimp snaps on restored hard-bottom were similar to those of healthy hard-bottom. Habitat quality and moon phase both significantly affected larval recruitment. Overall, healthy hard-bottom habitat attracted significantly more larvae than either degraded or restored hard-bottom, particularly during full moon. Playback of healthy hard-bottom soundscapes within degraded hard-bottom areas prompted higher larval settlement, particularly during the full moon. Estimates of snapping shrimp populations within degraded areas were significantly lower than estimates within healthy areas. Shrimp abundance estimates on healthy hard-bottom sites were one to two orders of magnitude greater than those on degraded sites. These studies demonstrate that tropical coastal habitats differ in soundscape characteristics, that habitat degradation affects soundscapes and the ecological process of larval settlement and recruitment, and that restoration of hard-bottom habitat can aid in returning these functions

Determining temporal sampling schemes for passive acoustic studies in different tropical ecosystems

Among different approaches to exploring and describing the ecological complexity of natural environments, soundscape analyses have recently provided useful proxies for understanding and interpreting dynamic patterns and processes in a landscape. Nevertheless, the study of soundscapes remains a new field with no internationally accepted protocols. This work provides the first guidelines for monitoring soundscapes in three different tropical areas, specifically located in the Atlantic Forest, Rupestrian fields, and the Cerrado (Brazil). Each area was investigated using three autonomous devices recording for six entire days during a period of 15 days in both the wet and dry seasons. The recordings were processed via a specific acoustic index and successively subsampled in different ways to determine the degree of information loss when reducing the number of minutes of recording used in the analyses. We describe for the first time the temporal and spectral soundscape features of three tropical environments. We test diverse programming routines to describe the costs and the benefits of different sampling designs, considering the pressing issue of storing and analyzing extensive data sets generated by passive acoustic monitoring. Schedule 5 (recording one minute of every five) appeared to retain most of the information contained in the continuous recordings from all the study areas. Less dense recording schedules produced a similar level of information only in specific portions of the day. Substantial sampling protocols such as those presented here will be useful to researchers and wildlife managers, as they will reduce time- and resource-consuming analyses, whilst still achieving reliable results

THE SOUNDSCAPE APPROACH FOR THE ASSESSMENT AND CONSERVATION OF MEDITERRANEAN LANDSCAPES: PRINCIPLES AND CASE STUDIES

Abstract The fine-grained mosaic of natural and human-modified patches that characterizes the Mediterranean region has created a multifaceted system that is difficult to investigate using traditional ecological techniques. In this context, sounds have been found to be the optimum model to provide indirect and timely information about the state of ecosystems. The sonic nature of the environment (the soundscape) represents an important component of the landscape, and the new discipline of soundscape ecology has recently been shown to have appropriate tools for investigating the complexity of the environment. In the last decade, technological advances in the acoustic field have led researchers to carry out wide-scale and long-term ecological research using new and efficient tools, such as digital low cost sound recorders, and autonomous software and metrics. Particularly in the Mediterranean region, where land transformation occurs at a very rapid rate, soundscape analysis may represent an efficient tool with which to:1) track transformations in the community balance, 2) indicate the most acoustically complex parts (bioacoustic hotspots) of the land mosaic, 3) prevent environmental degradation, and 4) decide whether protection or restoration actions are most appropriate. Conserving the quality of Mediterranean sounds means preserving the natural dynamics of its animal populations and also involves maintaining the cultural heritage, human identity, and the spiritual values of the area

INDICES AND ECOINFORMATICS TOOLS FOR THE STUDY OF SOUNDSCAPE DYNAMICS

The study of the new field of soundscape ecology presents several research avenues to explore. In the chapters in this dissertation, I have followed several of the technical and methodological areas of the study of soundscapes. In Chapter 1, I presented the current status of the study of soundscapes as well as an overview of the contributions made in this dissertation to the field. These contributions were framed in the definition of ecological informatics (Michener and Jones 2012). In Chapter 2, I developed a web-based system to manage audio archives. This system organizes thousands of audio files while collecting the necessary metadata

The Tallgrass Prairie Soundscape; Employing an Ecoacoustic Approach to Understand Grassland Response to Prescribed Burns and the Spatial and Temporal Patterns of Nechrophilous Invertebrate Communities

Tallgrass prairies are rapidly vanishing biodiversity hotspots for native and endemic species, yet little is known regarding how spatial and temporal variation of prairie soundscapes relates to seasonal changes, disturbance patterns and biological communities. Ecoacoustics, the study of environmental sounds using passive acoustics as a non-invasive tool for investigating ecological complexity, allows for long-term data to be captured without disrupting biological communities. Two studies were carried out by employing ecoacoustic methodology to study grassland carrion food webs and to capture the phenology of a grassland soundscape following a prescribed burn. Both studies were conducted at the Nature Conservancy’s Tallgrass Prairie Preserve (3650’N, 9625’W) and used six acoustic indices to quantify the ratio of technophony to biophony, acoustic complexity, diversity, evenness, entropy, and biological acoustic diversity from over 70,000 sound recordings. Acoustic index values were used to determine the relationship between Nicrophorus burying beetle species composition and the prairie soundscape (Chapter 1) and to determine if prescribed burning changes the composition of the soundscape over time (Chapter 2). In Chapter 1, I found that associations between Nicrophorus burying beetles and the soundscape were unique to particular species, acoustic indices and times of day. For example, N. americanus trap rates showed a positive correlation to areas of increased acoustic complexity specifically at dawn. In addition to positive associations with the soundscape, we found that N. marginatus was consistently negatively correlated to higher levels of biophony, while N. tomentosus was consistently positively correlated to places with higher levels of biophony. Although reproduction of all species examined is dependent upon securing small carrion for reproduction, I found that known habitat and activity segregation of five Nicrophorus beetle species may be reflective of the soundscape. Finally, I show that favorable habitat for a critically endangered necrophilous insect, the American burying beetle (Nicrophorus americanus) can be identified by the acoustic signature extracted from a short temporal window of its grassland ecosystem soundscape. Using the same suite of acoustic indices from Chapter 1, in Chapter 2 I examined acoustic recordings at a much larger time scale to determine distinctive acoustic events driven by biophony and geophony across a 23-week period. In addition to examining acoustic changes over time, I examined differences between 11 burned and unburned pastures. Results from this study indicate that prescribed burning does alter the soundscape, especially early in the post-burn period, but the effects are ameliorated by a significant increase in biophony as the growing and breeding season progressed into the warmer summer months. Both studies demonstrate that passive acoustic recording is a reliable method to assess relationships to acoustic communities over space and time

Determining temporal sampling schemes for passive acoustic studies in different tropical ecosystems

Among different approaches to exploring and describing the ecological complexity of natural environments, soundscape analyses have recently provided useful proxies for understanding and interpreting dynamic patterns and processes in a landscape. Nevertheless, the study of soundscapes remains a new field with no internationally accepted protocols. This work provides the first guidelines for monitoring soundscapes in three different tropical areas, specifically located in the Atlantic Forest, Rupestrian fields, and the Cerrado (Brazil). Each area was investigated using three autonomous devices recording for six entire days during a period of 15 days in both the wet and dry seasons. The recordings were processed via a specific acoustic index and successively subsampled in different ways to determine the degree of information loss when reducing the number of minutes of recording used in the analyses. We describe for the first time the temporal and spectral soundscape features of three tropical environments. We test diverse programming routines to describe the costs and the benefits of different sampling designs, considering the pressing issue of storing and analyzing extensive data sets generated by passive acoustic monitoring. Schedule 5 (recording one minute of every five) appeared to retain most of the information contained in the continuous recordings from all the study areas. Less dense recording schedules produced a similar level of information only in specific portions of the day. Substantial sampling protocols such as those presented here will be useful to researchers and wildlife managers, as they will reduce time- and resource-consuming analyses, whilst still achieving reliable results

Quantification of Marine Acoustic Environments

The soundscape is an acoustic environment made up of all sounds arriving at a receiver. A methodology for the analysis of soundscapes was developed in an attempt to facilitate efficient and accurate soundscape comparisons across time and space. The methodology included generating and combining results from a collection of traditional soundscape metrics, statistical measures, and acoustic indices that were selected to quantify several salient properties of marine soundscapes: amplitude, impulsiveness, periodicity, and uniformity. The metrics were calculated using approximately 30 hours using semi-continuous passive acoustic data gathered in seven unique acoustic environments. The calculated values for each candidate metric were compared to a priori soundscape descriptions and cross-examined statistically to determine which combination of metrics most effectively captured the characteristics of the representative soundscapes. The selected measures of were SPLrms and SPLpk for amplitude, kurtosis for impulsiveness, an autocorrelation-based metric for periodicity, and the dissimilarity index for uniformity. The metrics were combined to develop a proposed soundscape code, which enables rapid multidimensional and direct comparisons of salient soundscape properties across time and space. The proposed soundscape code was applied to a series of soundscapes that were recorded at several deep ocean environments along the US outer continental shelf (OCS) and the Great Barrier Reef. The soundscape code clearly distinguished between the deep OCS soundscapes and the shallow Great Barrier Reef soundscape in terms of amplitude, impulsiveness, and periodicity. Nuanced differences in deep OCS soundscape codes in terms of periodicity, impulsiveness, and the frequency of dominant signals suggest a connection between the respective soundscapes and bottom type or habitat. The combination of metrics that make up the soundscape code provided a first assessment to establish baseline acoustic properties for the deep ocean OCS sites. This initial soundscape characterization will aid in directing further analyses and guiding subsequent assessments used in understanding soundscape dynamics

Passive acoustic metrics to understand shallow water biodiversity off Malvan area in the west coast of India

527-536Underwater soundscape monitoring is an effective method to understand the biodiversity of an ecosystem. In this context, quantitative characterization of shallow water soundscape of the Burnt Island located off Malvan area in the west coast of India (WCI) is carried out. The soundscape characterization involves analysis of the “waveform”, “spectrogram”, and the “power spectral density” (PSD) of the recorded passive acoustic data. Biophonies such as the fish chorus of Terapon theraps, sparse calls of Carangidae along with another unnamed fish species community is reported. Evaluation of the PSDs and corresponding peak frequencies to distinguish the wave-breaking sound and fish species are also covered. Three acoustic metrics namely acoustic entropy (H), acoustic richness (AR), and acoustic complexity index (ACI) of passive acoustic recordings are computed and analyzed to understand their role in relation to fish chorus, wave-breaking, and sparsely available fish sound