Behavioral responses of common dolphins to naval sonar

Despite strong interest in how noise affects marine mammals, little is known about the most abundant and commonly exposed taxa. Social delphinids occur in groups of hundreds of individuals that travel quickly, change behavior ephemerally, and are not amenable to conventional tagging methods, posing challenges in quantifying noise impacts. We integrated drone-based photogrammetry, strategically-placed acoustic recorders, and broad-scale visual observations to provide complimentary measurements of different aspects of behavior for short- and long-beaked common dolphins. We measured behavioral responses during controlled exposure experiments (CEEs) of military mid-frequency (3-4 kHz) active sonar (MFAS) using simulated and actual Navy sonar sources. We used latent-state Bayesian models to evaluate response probability and persistence in exposure and post-exposure phases. Changes in sub-group movement and aggregation parameters were commonly detected during different phases of MFAS CEEs but not control CEEs. Responses were more evident in short-beaked common dolphins (n=14 CEEs), and a direct relationship between response probability and received level was observed. Long-beaked common dolphins (n=20) showed less consistent responses, although contextual differences may have limited which movement responses could be detected. These are the first experimental behavioral response data for these abundant dolphins to directly inform impact assessments for military sonars.

Methods
We used complementary visual and acoustic sampling methods at variable spatial scales to measure different aspects of common dolphin behavior in known and controlled MFAS exposure and non-exposure contexts. Three fundamentally different data collection systems were used to sample group behavior. A broad-scale visual sampling of subgroup movement was conducted using theodolite tracking from shore-based stations. Assessments of whole-group and sub-group sizes, movement, and behavior were conducted at 2-minute intervals from shore-based and vessel platforms using high-powered binoculars and standardized sampling regimes. Aerial UAS-based photogrammetry quantified the movement of a single focal subgroup. The UAS consisted of a large (1.07 m diameter) custom-built octocopter drone launched and retrieved by hand from vessel platforms. The drone carried a vertically gimballed camera (at least 16MP) and sensors that allowed precise spatial positioning, allowing spatially explicit photogrammetry to infer movement speed and directionality. Remote-deployed (drifting) passive acoustic monitoring (PAM) sensors were strategically deployed around focal groups to examine both basic aspects of subspecies-specific common dolphin acoustic (whistling) behavior and potential group responses in whistling to MFAS on variable temporal scales (Casey et al., in press). This integration allowed us to evaluate potential changes in movement, social cohesion, and acoustic behavior and their covariance associated with the absence or occurrence of exposure to MFAS. The collective raw data set consists of several GB of continuous broadband acoustic data and hundreds of thousands of photogrammetry images. 

Three sets of quantitative response variables were analyzed from the different data streams: directional persistence and variation in speed of the focal subgroup from UAS photogrammetry; group vocal activity (whistle counts) from passive acoustic records; and number of sub-groups within a larger group being tracked by the shore station overlook. We fit separate Bayesian hidden Markov models (HMMs) to each set of response data, with the HMM assumed to have two states: a baseline state and an enhanced state that was estimated in sequential 5-s blocks throughout each CEE. The number of subgroups was recorded during periodic observations every 2 minutes and assumed constant across time blocks between observations. The number of subgroups was treated as missing data 30 seconds before each change was noted to introduce prior uncertainty about the precise timing of the change. For movement, two parameters relating to directional persistence and variation in speed were estimated by fitting a continuous time-correlated random walk model to spatially explicit photogrammetry data in the form of location tracks for focal individuals that were sequentially tracked throughout each CEE as a proxy for subgroup movement.

Movement parameters were assumed to be normally distributed. Whistle counts were treated as normally distributed but truncated as positive because negative count data is not possible. Subgroup counts were assumed to be Poisson distributed as they were distinct, small values. In all cases, the response variable mean was modeled as a function of the HMM with a log link:

log(Responset) = l0 + l1Z t

where at each 5-s time block t, the hidden state took values of Zt = 0 to identify one state with a baseline response level l0, or Zt = 1 to identify an “enhanced” state, with l1 representing the enhancement of the quantitative value of the response variable. A flat uniform (-30,30) prior distribution was used for l0 in each response model, and a uniform (0,30) prior distribution was adopted for each l1 to constrain enhancements to be positive. For whistle and subgroup counts, the enhanced state indicated increased vocal activity and more subgroups. A common indicator variable was estimated for the latent state for both the movement parameters, such that switching to the enhanced state described less directional persistence and more variation in velocity. Speed was derived as a function of these two parameters and was used here as a proxy for their joint responses, representing directional displacement over time.         

To assess differences in the behavior states between experimental phases, the block-specific latent states were modeled as a function of phase-specific probabilities, Z t ~ Bernoulli (pphaset), to learn about the probability pphase of being in an enhanced state during each phase. For each pre-exposure, exposure, and post-exposure phase, this probability was assigned a flat uniform (0,1) prior probability. The model was programmed in R (R version 3.6.1; The R Foundation for Statistical Computing) with the nimble package (de Valpine et al. 2020) to estimate posterior distributions of model parameters using Markov Chain Monte Carlo (MCMC) sampling. Inference was based on 100,000 MCMC samples following a burn-in of 100,000, with chain convergence determined by visual inspection of three MCMC chains and corroborated by convergence diagnostics (Brooks and Gelman, 1998). To compare behavior across phases, we compared the posterior distribution of the pphase parameters for each response variable, specifically by monitoring the MCMC output to assess the “probability of response” as the proportion of iterations for which pexposure was greater or less than ppre-exposure and the “probability of persistence” as the proportion of iterations for which ppost-exposre was greater or less than ppre-exposure. These probabilities of response and persistence thus estimated the extent of separation (non-overlap) between the distributions of pairs of pphase parameters: if the two distributions of interest were identical, then p=0.5, and if the two were non-overlapping, then p=1. Similarly, we estimated the average values of the response variables in each phase by predicting phase-specific functions of the parameters:

Mean.responsephase = exp(l0 + l1pphase)

and simply derived average speed as the mean of the speed estimates for 5-second blocks in each phase.