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Lisa Palmer is a journalist and author of Hot, Hungry Planet: The Fight to Stop a Global Food Crisis in the Face of Climate Change (St. Martin’s Press, 2017), and the National Geographic Visiting Professor of Science Communication at the George Washington University in Washington DC. More

Study siteThis study took place at a temperate reef called the “Chicken Rock” in waters off the coast of North Carolina, USA, between Cape Hatteras and Cape Lookout (Raleigh Bay; Fig. 1). The seafloor of the Chicken Rock is composed of low-relief hardbottom and sand. The Chicken Rock is approximately 37 m deep (Fig. 2) and is an ideal location for this study for three reasons. First, it has a relatively flat seafloor that allows for a high detection rate of acoustically tagged fish49. Second, a high-resolution bathymetric map was available for the area (C. Taylor, National Centers for Coastal Ocean Science). Third, many red snapper occupy the area, allowing us to catch and tag fish relatively easily. Recreational and commercial fishing occurs at the Chicken Rock year-round for a variety of species, but red snapper can only be retained during short open seasons that have occurred periodically since 2010.Data collectionWe quantified the fine-scale movements and distance off bottom for red snapper using VPS (Innovasea, Nova Scotia, Canada). VPS uses a time-difference-of-arrival algorithm to determine the location of coded acoustic transmitters that have been detected by at least three submersible acoustic receivers50. Highly precise fish positions (~ 1 m resolution) are possible if time is synchronized exactly across all receivers, which is accomplished by using sync tags that are either deployed independently throughout the receiver array or built into the receivers themselves. One downside of VPS is that data are not available in real time; receivers must be physically recovered to download data, and then data have to be sent to Vemco to determine fish positions. The advantages of VPS, however, are immense, especially in providing highly precise spatial positions each time acoustic signals are emitted from transmitters. VPS has been used many times to successfully quantify demersal fish movements27,28,49,50,54, and three-dimensional movements can be determined if pressure sensors are built into transmitters23,42.We deployed an array of 20 submersible VR2AR receivers at the Chicken Rock on 17 April 2019. Receivers were deployed in three rows of seven receivers, except for a single receiver in the northeast corner of the grid. Based on previously estimated detection distances of 200–400 m49,55, receivers were separated 200 m from each other, so the entire receiver grid occupied an area of approximately 400 × 1200 m (0.48 km2; Fig. 2). Each receiver was connected to a line between a 36-kg steel weight and a 28-cm diameter plastic float with 8.8 kg of buoyancy, with each receiver positioned approximately 3 m off the seafloor. Each VR2AR included its own sync tag for time synchronization and acoustic release so receivers could be retrieved at the end of the study. A TCM-1 current probe (Lowell Instruments) was attached to each of three receiver buoys spread out across our receiver array (Fig. 2) to collect minute-by-minute current speed and bottom water temperature.We also deployed a reference transmitter (Vemco V13T-1x) in the receiver array on 17 April 2019 (Fig. 2) to calculate sound speed velocity for VPS analyses and quantify positional error of transmitters in the receiver array by comparing its known location to its estimated positions over the course of the study. The reference transmitter was connected to a line with a weight at one end and a buoy at the other, had a 550–650 s random ping interval, and operated on a frequency of 69 kHz.A total of 44 red snapper were tagged in this study. Twenty-three red snapper were tagged on 7 May 2019, nineteen were tagged on 13 August 2019, one was tagged on 30 August 2019, and one was tagged on 22 September 2019 (Table 1). Most of these red snapper (N = 43) were caught via hook-and-line using either circle or J-style hooks, but one red snapper (tagged on 30 August 2019) was caught in a baited fish trap. Fish in good condition (i.e., no visible signs of barotrauma, jaw hooked, active) were tagged externally because external attachment is fast (i.e., greatly reducing surface time56) and externally attached transmitters are detected better than surgically implanted transmitters57. The downside is that transmitter retention is typically lower for externally attached transmitters compared to surgically implanted transmitters.We tagged red snapper with Vemco V13P-1 × transmitters that were 13 mm wide, 46 mm long, weighed 13 g in air, had a 130–230 s pulse interval, a 613 d battery life, and operated on a frequency of 69 kHz. Each transmitter also contained a pressure sensor, which was used to determine the depth of fish for each acoustic signal (accuracy = 1.7 m). Before field work began, stainless steel wire (0.89-mm diameter) was wrapped around the non-transmitting end of the transmitter, glued with marine adhesive (3 M 5200), and covered in heat shrink tubing. Approximately 15 cm of stainless steel wire that extended beyond the transmitter was straightened, and the end was sharpened.Upon capture, red snapper had their head and eyes covered in a wet towel and were measured for total length (mm). The sharpened transmitter wire was inserted laterally through the dorsal musculature of the fish approximately 2.5 cm posterior to, and 2.5 cm below, the insertion of the fish’s first dorsal spine. The wire was pushed laterally through the fish until the transmitter was pulled firmly against the fish’s left side, while the sharpened end emerged from the same spot on the right side of the fish. An aluminum washer was threaded onto the protruding wire, followed by a #1 double sleeve steel crimp, which was crimped onto the wire once the washer and crimp were held firmly on the right side of the fish. The wire beyond the crimp and wet towel were removed, the fish was attached to a weighted SeaQualizer fish release tool, and the fish was descended to a depth of approximately 31 m before being released by the device. The total surface time for each tagged red snapper was approximately 1.5 min.Data analysesWe first assessed whether potential error in red snapper positions could influence study results. For each reference tag position estimated by VPS, we calculated horizontal positional error as the difference between the known reference tag location and its estimated position based on VPS. We visualized daily horizontal positional error of the reference transmitter with a boxplot. Daily values were provided to determine if any changes in positional error occurred over time.Next, we used positional and depth data from fish that were monitored to determine the fate of each individual and classified them based on four events: tag loss, emigration, harvest, or predation48. Fish were assumed to have lost transmitters if the transmitter stopped moving; they were assumed to have emigrated if the transmitter moved to the edge of the receiver array before disappearing. Harvest was assumed if fish disappeared from within the receiver array. Predation (e.g., by sharks) was inferred from VPS data in one of three ways: (1) transmitters moved horizontally much faster than normal red snapper swimming speeds, (2) transmitters moved quickly across a wide range of depths, typically from the bottom to the surface and back, and (3) a reduced frequency of detections, as might be expected for transmitters in the abdominal cavity of a shark. VPS data were censored after the point at which any fish experienced tag loss, harvest, or predation, and only fish with 100 or more spatial positions were included in the analyses.We then estimated movement rates of each fish over time. Movement rate (m s−1) was quantified as the distance moved between each successive pair of spatial positions divided by the time between detections. One challenge with using movement rates is that straight-line movements are assumed between detections, when in reality fish may not move in straight lines. Red snapper were detected on average every 2–4 min, so this issue is less of a problem in our study compared to those using longer time intervals between detections51, but our movement rates can be considered minimum estimates. To further prevent negatively biased movement rate estimates, we excluded movement rate estimates for time intervals longer than 20 min; this decision had negligible effects on results (see Discussion).We also estimated the distance off the seafloor for all detections of acoustically tagged red snapper. We calculated distance off the bottom (m) for each fish position as the depth of the seafloor at that location minus the depth of the fish. We encountered an issue with some transmitters after tag loss whereby depth readings appeared to slowly drift towards shallower readings even though the transmitter was sitting on the bottom and not moving horizontally; in a few instances, this same depth drift issue was detected for transmitters attached to fish alive in the study area (i.e., distance off bottom was greater than zero for long periods of time, which never occurred for red snapper with working pressure sensors). We do not know the reason for these rare instances of depth drift by the pressure sensors, but out of caution we censored depth data for fish whose transmitters provided dubious depth data.We evaluated whether individual differences in movement rates or distance off the bottom were apparent. We created boxplots of movement rate and distance off bottom for each fish in the study, and tested for differences among individuals using a linear model where fish number was included as a categorical variable. We compared the Akaike information criterion (AIC) values of models including fish number with an intercept-only model where fish number was excluded, and models with the lowest AIC value (ΔAIC = 0) were considered the most parsimonious formulations58. Movement rate was positively skewed, so it was log-transformed to improve model fit. Model diagnostics (i.e., quantile–quantile, histogram of residuals, residuals versus linear predictions, response versus fitted values plots) were used to confirm that final models met assumptions of equal variance and normal residuals. We used R version 3.6.359 to carry out all statistical tests and to create all figures.Ideally, we would then test for the effects of environmental conditions and fish size on red snapper horizontal and vertical movements using a single, integrated analysis. However, models accounting for temporal autocorrelation and incorporating individual movement rate estimates from each fish as the response variable (i.e., including fish number as a random effect) did not converge, possibly due to large sample sizes (N = 346,363), so we used mean hourly values instead. The downside of this approach is that fish size had to be evaluated separately from the effects of environmental conditions, as described below. However, note that covariate relationships changed very little across a wide variety of model formulations.We tested for the effects of fish size on movement rate and distance off the bottom using generalized additive models60 (GAMs). GAMs are a regression modeling approach that relate a response variable to a single or multiple predictor variables using nonlinear, linear, or categorical functions. Mean log-transformed movement rate or distance off bottom were the response variables of these models and cubic-spline-smoothed fish total length (mm) was included as the predictor variable. As above, we compared the AIC values of models including fish size with an intercept-only model where fish size was excluded, and the model with the lowest AIC value was selected as the best model.We then assessed the influence of various environmental factors (see below) on red snapper movement rate and distance off bottom using GAMs. For these analyses, choosing the appropriate time scale for binning response and predictor data was critical. Longer time steps (i.e., day) were problematic because response and predictor variables frequently varied over much shorter time frames, while extremely short time steps (i.e., minute) were often lacking response and predictor variable information. Therefore, we used an hourly time step for this procedure. The main concern of using an hourly step is that any particular hourly time bin is likely to be more similar to the time bin nearest in time compared to a randomly selected time bin; in other words, time bins are not truly independent of one another61 (i.e., data are temporally autocorrelated). Not accounting for temporal autocorrelation that is present often leads to a negative bias in estimated regression coefficients and confidence intervals. To account for temporal autocorrelation, we used generalized additive mixed models (GAMMs) that included an autoregressive term for model errors. We used a likelihood ratio test to compare our GAMM to a GAM that did not include autoregressive errors, and in both cases GAMMs were selected over GAMs so they were used for movement and distance off bottom models.We limited our GAMMs to five predictor variables based on previous work. The first predictor variable was time of day, which we included because red snapper movements have been shown to vary over diel periods29. We included time of day (tod) as a categorical variable with three levels: day, crepuscular period, and night. Because sunrise and sunset times varied over the course of our 8-mo study, we defined crepuscular periods as a one hour period of time spanning 30 min before sunrise or sunset to 30 min after sunrise or sunset for each day of the study. Day was defined as 30 min after sunrise to 30 min before sunset, and night was defined as 30 min after sunset to 30 min before sunrise.Bottom water temperature has been shown to be strongly correlated with red snapper movements and home range size28,29, so it was included as our second predictor variable. We calculated bottom water temperature (temp; °C) as the mean bottom temperature measured across the three current probes deployed in the receiver array. Cold bottom water temperatures were observed near the conclusion of our study (December 2019) due to declining air temperatures and water column mixing, but also during periodic upwelling events that occurred from late May through early August. Upwelling is a common oceanographic feature of the region, occurring when upwelling-favorable winds are observed concurrent with the Gulf Stream being in a relatively inshore position62,63. Upwelled water that is cold and nutrient-rich is generally only found near the bottom, which tends to cause phytoplankton blooms near the bottom that decrease water clarity. From preliminary analyses of red snapper VPS data, we observed differing behaviors of fish during periods of upwelling than periods lacking upwelling. Therefore, we developed an upwelling index as our third predictor variable, which was calculated as the difference between the surface water temperature and mean bottom water temperature (upwel; °C). Surface water temperature was not available at the study site, so we obtained hourly surface temperature data from the nearest NOAA buoy (#41159), which was located ~ 85 km southwest of the study site in a similar water depth (Fig. 1). We assume that surface water temperature at the study site could be approximated with data from this buoy, which is a reasonable assumption given surface water temperature and wave heights from this buoy were strongly correlated with values from another buoy (NOAA buoy #41025) ~ 70 km northeast of the study site.The last two predictor variables involved properties of water movement at the seafloor in the study area. The fourth predictor variable was wave orbital velocity (wov; m s−1), which is a measure of the wave-generated oscillatory flow (“sloshing”) of water at the seabed. Wave orbital velocity was included because it was much more strongly correlated with gray triggerfish (Balistes capriscus) movement rates at the Chicken Rock area than either barometric pressure or bottom water temperature43, the latter of which have been shown to be more important for organisms in shallow water64,65. Wave orbital velocity was calculated following Bacheler et al.43 using the properties of surface wave period and height, which were also obtained from NOAA buoy 41159. The last predictor variable included in models was current speed (cur; cm s−1), which was calculated as the mean horizontal current speed from the three current probes deployed on the bottom in the receiver array.The GAMMs were formulated as:$$y = upalpha + f(tod) + s_{1} (temp) + s_{2} (upwel) + s_{3}(wov) + s_{4} (cur) + varepsilon ,$$
(1)
where y is either acoustically tagged red snapper log-transformed movement rate (m s−1) or distance off the bottom (m), α is the intercept, f is a categorical function, s1-4 are cubic spline smoothing functions, and (varepsilon) is the autoregressive error term accounting for temporal autocorrelation in the data.We employed model selection techniques to assess the importance of predictor variables. Specifically, we compared full models that included all five predictor variables to reduced models that included fewer predictor variables. Model comparisons were made using AIC, and models with the lowest AIC value (ΔAIC = 0) were again considered the most parsimonious. Various diagnostics of final models were examined using the “gam.check” function in the mgcv library to ensure model fit was suitable.Given the importance of upwelling to the vertical movements of red snapper (see Results section), we last include results from a conductivity-temperature-depth (CTD) cast taken in the study area from the NOAA Ship Pisces on 29 June 2019 (07:40 EDT), which occurred during a time when bottom upwelling was present. This CTD cast was conducted using a Sea-Bird SBE 9 deployed from the surface to within 1.5 m of the bottom, and depth-specific water temperature and beam transmission data were provided to highlight the vertical extent of upwelling on this particular day. Beam transmission is the fraction of a light source reaching a light detector set a distance away and is a quantitative measure of water clarity; a common feature of upwelling in the region (in addition to cold water) is declining clarity due to increased production within nutrient-rich, upwelled water near the bottom. We combine these water temperature and beam transmission data with a boxplot of red snapper distances off the bottom by hour throughout the same day the CTD cast was taken (29 June 2019).Ethics approvalThe tagging protocol was approved by the Institutional Animal Care and Use Committee (# NCA19-002) of the North Carolina Aquariums on 20 March 2019. All research activities were carried out under a Scientific Research Permit issued to Nathan Bacheler on 10 April 2017 by the Southeast Regional Office of the U.S. National Marine Fisheries Service, in accordance with the relevant guidelines and regulations on the ethical use of animals as experimental subjects. More

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