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Movement patterns of juvenile Atlantic tarpon (Megalops atlanticus) in Brewers Bay, St. Thomas, U.S. Virgin Islands

Movement patterns of juvenile Atlantic tarpon (Megalops atlanticus) in Brewers Bay, St. Thomas,... Background: Atlantic tarpon (Megalops atlanticus) are a highly migratory species ranging along continental and insular coastlines of the Atlantic Ocean. Due to their importance to regional recreational and sport fisheries, research has been focused on large-scale movement patterns of reproductively active adults in areas where they are of high economic value. As a consequence, geographically restricted focus on adults has left significant gaps in our under - standing of tarpon biology and their movements, especially for juveniles in remote locations where they are common. Our study focused on small-scale patterns of movement and habitat use of juvenile tarpon using acoustic telemetry in a small bay in St. Thomas, US Virgin Islands. Results: Four juvenile tarpon (80–95 cm FL) were tracked from September 2015 to February 2018, while an addi- tional eight juveniles (61–94 cm FL) left the study area within 2 days after tagging and were not included in analysis. 2 2 Four tarpon had > 78% residency and average activity space of 0.76 km (range 0.08–1.17 km ) within Brewers Bay (1.8 km ). Their vertical distribution was < 18 m depth with occasional movements to deeper water. Activity was greater during day compared to night, with peaks during crepuscular periods. During the day tarpon used different parts of the bay with consistent overlap around the St. Thomas airport runway and at night tarpon typically remained in a small shallow lagoon. However, when temperatures in the lagoon exceeded 30 °C, tarpon moved to cooler, deeper waters outside the lagoon. Conclusion: Our results, although limited to only four individuals, provide new baseline data on the movement ecol- ogy of juvenile Atlantic tarpon. We showed that juvenile tarpon had high residency within a small bay and relatively stable non-overlapping daytime home ranges, except when seasonally abundant food sources were present. Fine- scale acoustic tracking showed the effects of environmental conditions (i.e., elevated seawater temperature) on tar - pon movement and habitat use. These observations highlight the need for more extensive studies of juvenile tarpon across a broader range of their distribution, and compare the similarities and differences in behavior among various size classes of individuals from small juveniles to reproductively mature adults. Keywords: Acoustic telemetry, Home range, Vertical movement, Diel movement, Environmental effects Background Tracking the movements and migrations of animals in the aquatic environment provides insight into spatial and tem- *Correspondence: marapp15@gmail.com poral patterns of habitat use, trophic interactions, reproduc- Center for Marine and Environmental Studies, University of the Virgin tive behavior, and behavioral responses to environmental Islands, 2 John Brewers, US Virgin Islands, St. Thomas 00803, USA Full list of author information is available at the end of the article change [1–7]. Recent studies have shown that some highly © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 2 of 14 migratory species can exhibit high site fidelity to discrete mostly soft muddy bottom with scattered rocks and dead nearshore areas between migratory events, whereas rela- corals. It is partly enclosed by the airport runway with tively site-attached species can undergo repeated large-scale the remaining shoreline composed of rocky reef or soft migrations for reproduction [1, 8–10]. Integrating these sediments, and red mangroves (Rhizophora mangle). variable patterns of large-scale movements and small-scale activity spaces are becoming increasingly important for Acoustic array implementing ecosystem-based fisheries management, The acoustic monitoring system consisted of 45 omnidi - understanding connectivity, and designing ecologically rel- rectional receivers (VR2W, 69  kHz, Innovasea Systems evant marine managed areas [5, 11, 12]. Inc. (previously Vemco), Halifax, Nova Scotia, Canada) Atlantic tarpon (Megalops atlanticus) is a highly mobile that were moored, and spaced equally across Brewers Bay, pelagic species that supports important recreational and including eastern Perseverance Bay, and along the southern sport fisheries. Tarpon range across coastal areas, estuaries, side of the airport runway (Fig. 1). Range testing of receiv- and rivers of the western and eastern Atlantic Ocean, the ers [24] across the study site was conducted over four days Caribbean Islands, and the Gulf of Mexico [6, 13, 14]. Tar- in June 2015, by placing receivers in depths ranging from pon spend their larval stage as leptocephali in open ocean, 5 to 19  m over different substrate types including shallow and as juveniles settle nearshore in tropical and subtropi- and deep coral/rock and seagrass/sand [25]. Probabilities cal estuarine, mangrove and lagoon habitats, where food of transmission were tested using three A69-1601 Inno- resources are high and predator pressures are low [15–18]. vaSea transmitters V9-2H (151  dB), V13-1H (153  dB) and Adult tarpon range in size from 90–250  cm fork length V16-4H (158  dB) that transmitted every 60  s. Transmit- (FL) and males reach sexual maturity at about 90 cm while ters were attached to mooring lines, connected to cinder females at 128 cm FL [13, 19–21]. Much of our knowledge blocks, and suspended 1 m above the bottom. A detection of tarpon movements and behaviors come from satellite probability of 70% for V13-1H transmitters was selected tracking and conventional anchor tag studies conducted in providing high coverage throughout the study area with Florida, southeast Atlantic, Gulf of Mexico, and the north- estimated detection ranges of 101  m in seagrass/sand and western Caribbean (e.g., Mexico, Belize, Cuba) [6, 7, 13, 14, 120 m in coral/rock substrates (Fig.  1). Seawater tempera- 22, 23]. These studies have focused on large-scale move - ture and dissolved oxygen (DO) were collected at several ments (> 500 km) of large adult tarpon (> 130 cm FL) that stations in Brewers Bay using Hobo temperature loggers support a valuable sport fishery. The focus on adult tarpon (Onset Computer Corporation, Bourne, MA, USA) and over a limited geographic range leaves large gaps in our miniDot DO loggers (Precision Measurement Engineering understanding of tarpon biology and movement ecology, Inc, Vista, CA, USA) that were attached to acoustic receiver especially in insular areas throughout the eastern Carib- moorings. Temperature loggers were deployed in August bean where they are common [13]. We applied acoustic 2015, DO loggers were deployed in February 2016, and telemetry to quantify activity space, rates of movement, both recorded data at 15-min intervals (Fig. 1). vertical distribution and habitat use of juvenile tarpon across diel and seasonal time scales. Additionally, we exam- Fish capture ined how environmental conditions (i.e., water tempera- All capture and tagging methodology in Brewers Bay was ture, dissolved oxygen) influenced their behavior. approved by the University of the Virgin Islands Institu- tional Animal Care and Use Committee (IRB #747807- Materials and methods 1). Juvenile Atlantic tarpon were caught using hook and Study site line from a boat or dock between September 2015 and Brewers Bay is located on the western end of St. Thomas, November 2016. As each fish was reeled in, it was guided U.S. Virgin Islands (18°20′28″N, 64°58′40″W) and is alongside the boat or dock and into a floating cradle bounded by a commercial airport runway and small constructed of PVC pipe, plastic mesh, and foam noo- lagoon on the south, a sandy beach on the north-east- dles for buoyancy. Once in the cradle, the fish was held ern shore, and a rocky headland and smaller bay (Per- under water, turned upside-down to induce tonic-immo- severance Bay) to the northwest (Fig.  1). Brewers Bay is bility, and the hook was removed from the mouth. Each 1.8 km in area, ranges in depth between 0 and 33.1  m fish ( n = 14) was measured for fork length (FL) and total (Fig.  1), and has steep vertical slopes along the airport length (TL) to the nearest millimeter (mm). Acoustic runway and around the rocky headland. The bay is com - transmitters (either V13 [13 mm × 36 mm; n = 8] or V13P posed of a variety of habitat types including sand, sea- [13 mm × 46  mm; n = 6; pressure tags that provide depth grass, patch reefs, fringing coral reefs, rocky reefs, and data], 69 kHz, Innovasea Inc, Halifax, NS, Canada) were rubble and reinforced concrete blocks (dolosse) around surgically implanted into the body cavity on the ventral the seaward slopes of the airport runway. The lagoon is side of the fish [26]. The incision was closed with surgical D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 3 of 14 Fig. 1 Map of the Caribbean (a) and the island of St. Thomas in the US Virgin Islands (b) and study site in Brewers Bay (c) depicting bathymetry and the acoustic array with station number and approximate range of 70% detection probability (circles). Detection ranges varied by habitat (deep hard bottom = 115 m, deep soft bottom = 120 m, shallow soft and hard bottom = 101 m) based on range testing. Location of environmental data logger stations shown as green dots (temperature) and red diamonds (dissolved oxygen). Yellow dots represent approximate location where juvenile Atlantic tarpon were tagged and released. Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 4 of 14 staples and treated with antibacterial ointment (note: Temporal data were examined for seasonal and diel pat- antibacterial ointment is no longer used on incision and terns. Seasons were defined as spring (March, April, May), sutures). Fish remained immersed in open seawater the summer (June, July, August), fall (September, October, entire time so no general or local anesthetic was admin- November) and winter (December, January, February). istered, which allowed for the release of fish shortly after Crepuscular periods were calculated using astronomi- tagging and data collection were completed. Fish were cal twilight based on daily sunrise/sunset  time charts for turned back over, the head was faced into the current to Charlotte Amalie, St. Thomas, U. S. Virgin Islands [28]. increase ventilation, and after a few minutes of recovery, Specifically, dawn was defined as − 1 h before astronomi- fish were released at the capture location (Fig. 1). cal morning and + 1 h after sunrise to account for seasonal changes in day length. Likewise, dusk was defined as  − 1 h Data processing before astronomical twilight to + 1 h after sunset. Day and Detections were downloaded from receivers every 3 night periods were the remaining  hours between brack- months and analyzed using R Version 3.4.3 [27]. For each eted dawn and dusk, respectively. tarpon (n = 14) the total number of detections, first/last day detected, number of days between first and last day, and total days detected were calculated. Detections for Data analysis and statistics each individual tarpon by receiver were plotted through Residency index was calculated for the four fish used in time to investigate the presence of dropped tags, dead indi- analyses by dividing total days each fish was detected viduals, and short-term residency. Of the 14 juvenile tar- within the Brewers Bay array by number of days between pon that were tagged, four (n = 4) individuals had at least the first and last detection. Residency Index was defined 1  month of tracking data to conduct spatial home range as the percentage of days spent within Brewers Bay array analysis. Three of these tarpon were detected for 344–472 for the duration of time that each fish was tracked. days and also had pressure transmitters, thus were used Center of activity (COA) for juvenile tarpon (n = 4) was to analyze monthly and seasonal trends in rates of move- calculated every 30  min using mean position (latitude ment, activity space, and vertical distribution (Table 1). Of and longitude) of all detections during that time step [29]. the remaining ten tarpon that were excluded from analy- Distance between COA relocation points and difference sis, eight (n = 8) were within the array two days or less and in time between each relocation point were calculated had insufficient detections for analyses, and two (n = 2) for each fish using ‘adehabitatLT’ package of R environ - had either died or shed their tags (Table 1). ment [30]. COA values were used to calculate rate of Table 1 Summary data for Atlantic tarpon (M. atlanticus) caught and tracked in Brewers Bay acoustic array, including date caught (mm/dd/yyyy), total length ( TL), fork length (FL), total number of detections and total residency time detected in Brewers Bay Fish ID Tag date TL (cm) FL (cm) Total First day Last day Days between Total days Residency detections detected detected first and last detected index (%) detection 36032 9/17/2015 109 95 12231 9/17/2015 10/19/2015 32 28 88 10980P 6/17/2016 96 80 54564 6/18/2016 5/28/2017 344 330 96 10979P 6/26/2016 112 95 106564 6/26/2016 7/1/2017 370 287 78 2966P 10/25/2016 96 85 395606 10/26/2016 2/10/2018 472 464 99 36034 10/16/2015 90 78 326110 10/16/2015 7/11/2016 269 271 n/a 36036 10/21/2015 130 91.2 2017 10/22/2015 1/25/2016 95 74 n/a 59272 1/12/2016 86.4 76.1 10 1/12/2016 1/13/2016 1 1 n/a 36044 5/24/2016 70 61 5 5/24/2016 5/24/2016 1 1 n/a 36045 6/1/2016 130 91.2 14 6/1/2016 6/1/2016 1 1 n/a 2965P 8/8/2016 96 85 70 8/9/2016 8/9/2016 1 1 n/a 2964P 8/14/2016 100 80 11 8/14/2016 8/14/2016 1 1 n/a 36039 8/16/2016 100 94 10 8/16/2016 8/16/2016 1 1 n/a 2963P 9/15/2016 92 77 660 9/16/2016 9/17/2016 2 2 n/a 24976 10/29/2016 96 83 212 11/8/2016 11/8/2016 1 1 n/a P acoustic pressure transmitter measured depth, n/a not applicable Fish used for Brewers Bay spatial analyses Transient fish not used in spatial analyses Fish died or shed tag D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 5 of 14 movement (ROM) and activity space for individual fish, points. Kruskal–Wallis and Tukey post hoc tests were and included minimum convex polygons (100% MCP) used to test for differences in ROM between diel periods and kernel utilization distributions (50% and 95% KUD). and a two-way ANOVA was used to test for differences in Activity space, which incorporates MCP, 50% KUD and diel ROM across seasons. ROM provides a useful metric 95% KUD, was calculated using the ‘move’ and ‘adehabi- for fish activity during diel periods and can also be used tat’ package in R environment [30, 31]. MCPs provided as a proxy for feeding behavior [47]. information on the extent of an individual’s range or Vertical distribution was calculated for tarpon tagged area used and included all outlying points that might be with depth-enabled transmitters (n = 3, Table  1). Depth the result of exploratory movement or periodic migra- measurements were binned into hourly and monthly tion not part of their typical activity. KUDs highlight the periods and boxplots were applied to elucidate their ver- density of positions of an individual within the activity tical movement patterns. ANOVA and Tukey post hoc space based on COAs (i.e., 50% KUD = high density, 95% tests were used to test for differences in vertical move - KUD = low density), as well as estimated error around ment across diel and monthly periods. these positions [32, 33]. When necessary, a ‘land’ barrier Environmental conditions and their relationship to polygon was used to clip out the area of MCP and KUD tarpon movement and habitat use were assessed for sea- polygons that fell on land (‘rgeos’ package, [34]). The cal - water temperature and DO. Daily average number of culated MCP and KUD (50% and 95%) activity spaces detections, average temperature and average DO within were plotted in ArcGIS 10.6 for annual, monthly, and diel the lagoon and waters along the airport runway were periods. To calculate the degree of overlap in 50% and analyzed by applying a linear regression for the study 95% KUD among individuals over diel and monthly time period (September 2015—February 2018). periods, a home range (HR) percent overlap analyses was applied using the ‘kerneloverlaphr’ function of the ‘ade- Results habitatHR’ package [30, 35, 36]. The HR percent overlap Fourteen (n = 14) juvenile tarpon were captured and analyses calculates the proportion of animal a’s home acoustically tagged in Brewers Bay (average FL 83.7  cm, range that is overlapped by animal b’s home range [30, 35, range 61–95 cm; Table 1). Only four (n = 4) juvenile tarpon 36]. The data output matrix provides indices of overlap provided a sufficient number of detections over a sufficient for all pairs of animals [35, 36]. Using the matrix output, duration (32–472 days), and a residency index of 78–100%, average and ranges in fish overlap values were calculated. to be included in our spatial analysis (Table 1). Eight (n = 8) Repeated measures analyses of variance (RM-ANOVA) s fi h were detected for less than a week and had fewer than was used to test for differences in KUD across monthly 1000 detections and upon assessment, it was determined and diel periods. All monthly analyses used data from that the two remaining fish detected within the bay had three (n = 3) tarpon that had average KUD activity space died or shed their tags within one day following release. representing each month (Table  1). Individual tarpon were treated as random variables, and either monthly Activity space or diel periods were treated for autocorrelation effects The activity space of juvenile tarpon varied among indi - (‘corAR1’) using the ‘lme’ function of the ‘nlme’ package viduals and through time. The average MCP for juve - for R [37, 38]. To assess relationship between monthly 2 2 nile tarpon (n = 4) was 0.97 k m (range 0.77–1.17 k m ), ROM and 50% KUD size, a linear regression was applied. 2 while the average 95% and 50% KUD was 0.76 km (range Rate of movement (ROM, m/s) was calculated by divid- 2 2 2 0.49–0.99 km ) and 0.13 k m (range 0.08–0.20 k m ), ing the distance between consecutive COA position val- respectively (Table  2; Fig.  2). Comparison of mean day, ues by the time difference between these consecutive Table 2 Calculated home range size (km ) for each tarpon based on 50% and 95% Kernel utilization distribution (KUD) and 100% minimum convex polygon (MCP); number of center of activity (COA) points that fell on land and total percentage of COA points on land removed out of total COA points used for home range analyses Fish ID Total COA points MCP 100% area KUD 95% area KUD 50% area COA points on Percentage 2 2 2 (km ) (km ) (km ) land of COA points removed 2966 19,367 1.174 0.988 0.200 123 0.64 10979 11,888 1.055 0.619 0.075 163 1.37 10980 10,425 0.864 0.492 0.090 166 1.59 36032 887 0.767 0.938 0.149 7 0.79 In this case 100% MCP is smaller than 95% KUD based on how they are calculated (see “Materials and methods”) Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 6 of 14 Fig. 2 Activity space of juvenile tarpon (n = 4) based on yearlong 100 % MCP (black line in left panels), and 50% and 95% KUD for day (yellow/ orange left panels), night (blue/green right panels), and crepuscular (dawn = red, dusk = blue middle panels) time periods. The arrow represents an example of a corridor between day and night activity space. See Fig. 1 for labels. D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 7 of 14 Table 3 Summary of 50% and 95% Kernel utilization distribution (KUD) overlap for juvenile tarpon (n = 3) during day and night for full year, May to March (April excluded) and only April Month(s) Diel period KUD 50% area ± SE KUD 50% area range KUD 95% area ± SE KUD 95% area 2 2 2 2 (km ) (km ) (%) (km )range (km ) (%) All year Day 12% ± 6% 0–27 42% ± 12% 11–72 All year Night 20% ± 18% 0–99 51% ± 8% 28–99 May–March Day 2% ± 2% 0–6 23% ± 14% 8–55 May–March Night 19% ± 18% 0–99 44% ± 10% 14–99 April Day 20% ± 16% 1–55 63% ± 4% 42–74 April Night 10% ± 9% 0–32 33% ± 19% 11–81 night and crepuscular activity spaces among juvenile tar- 05:00 and at 18:00 (Fig.  3a). ROM was not significantly pon for both 50% and 95% KUDs were not significantly different across months (mean = 0.07 m/s ± 0.01 SD), but different across diel and crepuscular periods (50% KUD: there was a strong relationship between monthly ROM p = 0.07; 95% KUD: p = 0.44) and across months (50% and 50% KUD (F = 34.07, P = 0.0001, R = 0.77) with the KUD: p = 0.78; 95% KUD: p = 0.29). highest rates for both metrics during the months of April, Analysis of daytime activity space overlap averaged June and September (Fig. 3b). 12% for 50% KUD and 42% for 95% KUD during the year (Table  3), with each tarpon showing distinct 50% KUD Vertical movement core areas centered around northwest corner of runway Vertical movement of juvenile tarpon with pressure trans- (ID#36032), around Black Point and deeper part of Brew- mitters (n = 3) varied among time of the day (ANOVA: ers Bay (ID#2966), in and around the lagoon and Range F = 36,526, P < 0.0001) (Fig. 4). Tarpon used more of the 1,3 Cay extending to shallow and deep parts of Brewers Bay water column during the day ranging between 2 to 13 m (ID#10979), and around the tip of runway (ID#10980) average depth and 16 to 27  m maximum depth (Fig.  4). (Fig.  2, day). In April, however, overlap for 50% and 95% At night, tarpon stayed in shallower waters ranging from KUD during daytime showed an increase to 20% and 0 to 5  m average depth and 8 to 14  m maximum depth 63%, respectively (Table 3). Excluding the month of April, (Fig.  4; Additional file  1: Table  S1). Nighttime vertical daytime 50% and 95% KUD overlap values declined from movements were partly constrained when tarpon were in 12 to 2% and 42% to 23%, respectively (Table 3). At night- lagoon (maximum depth 4  m, Fig.  2). During dawn and time, 50% KUD areas were centered in shallow Brewers dusk, average depth of tarpon ranged between 0 to 8  m Bay, around the airport runway and particularly inside (Fig.  4; Additional file  1: Table  S1). Vertical distribution the shallow lagoon, where juvenile tarpon went at night across months showed no consistent patterns among the (Fig.  2, night). Consistent use of these areas at night three tarpon with depth transmitters. tended to increase nighttime 50% and 95% KUD overlap relative to daytime, except for April, when space overlap Movement and environmental variability decreased at night (Table 3). Water temperature in Brewers Bay ranged from 25–28 °C in winter to 29–32  °C in late summer and early fall. Rate of movement Inside the lagoon water temperature showed greater Average ROM of juvenile tarpon was 0.07  m/s fluctuations on a daily basis and had a greater range (± 0.02 SD) and was significantly different among (mean = 28.3  °C ± 1.27 SD, range = 24.8–32.0 °C) than in diel periods (H = 12.4, P < 0.006). Post hoc com- the bay (mean = 28.1  °C ± 1.15 SD, range = 25.6–30.6  °C) parisons between day (mean = 0.06  m/s ± 0.01 (Fig.  5). Water temperature had a strong effect on tar - SD), night (mean = 0.05  m/s ± 0.01 SD), pon movement and habitat use. We found a significant dawn (mean = 0.09  m/s ± 0.01 SD) and dusk negative relationship between number of tarpon detec- (mean = 0.10  m/s ± 0.01 SD) showed a significant differ - tions and temperature in the lagoon at night (adjusted ence between dusk and nighttime periods only (Tukey R = 0.0.32; P < 0.001), but no relationship between fre- HSD: P < 0.01). Diel ROM also varied across seasons quency of detections in the lagoon or around the runway (2-way ANOVA: F = 253.2, P < 0.0001). Most notable, at other times of day (Fig. 6). Juvenile tarpon were present 1,15 daytime ROM was significantly lower in winter com - in the lagoon at night when temperature ranged between pared to other seasons (Tukey HSD: P < 0.001). During 26 and 28  °C; however, once temperature reached 29  °C all seasons, crepuscular ROM peaked between 04:00 to frequency of tarpon detections decreased rapidly and Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 8 of 14 Fig. 3 a Diel ROM of juvenile tarpon by season of the year: Spring (March, April, May), Summer (June, July, August), Fall (September, October, November) and Winter (December, January, February). b Relationship between average ROM and core activity space 50% KUD for four juvenile tarpon during each month stopped at about 30.5  °C (Fig.  6), indicating tarpon left 249, 285, 251, 282; Fig.  1), where nighttime maximum the lagoon. Water temperatures in the lagoon reached or water temperatures were cooler (Figs. 5, 6a). When water exceeded 30.5 °C on 59 day of the study period compared temperatures in lagoon cooled to below 30.5 °C, juvenile to only 4 days at the airport runway. Likewise, water tem- tarpon returned to resting in lagoon at night (Fig. 5). peratures 26  °C colder were recorded on 61 day in the Similar to water temperature, dissolved oxygen concen- lagoon but only on 16 day along runway. At times of high trations in the lagoon varied widely from 0.9 to 7.1 mg/L lagoon temperatures, juvenile tarpon left the lagoon and (mean = 4.7 ± 1.89 SD), but were more stable along had higher frequency of detections at night along the tip the airport runway (mean = 6.1 ± 1.9 SD, range 5.3– and south side of the airport runway (i.e., stations 248, 6.6 mg/L) (Fig.  5). Based on detection frequencies, there D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 9 of 14 Fig. 4 Boxplot of daily distributions by hour of vertical movement of three juvenile tarpon during diel (day, night) and crepuscular (dawn, dusk) periods was no significant relationship in number of detections and November) before returning to its home range of tarpon at different levels of dissolved oxygen within for another 7  months. The second tarpon (ID#3032) the lagoon or the runway (Fig. 6b), indicating that tarpon remained within Brewers Bay for 1 month before depart- seemed to tolerate the low oxygen levels in the lagoon, ing mid-October, but it was then detected at an acoustic especially at night array 12  km offshore in January. Interestingly, both tar - pon departed in October when water temperature was high. Seasonal movements, such as these, by Atlantic Discussion tarpon and other coastal species have been attributed to To our knowledge, this study provided some of the first food availability, reproductive maturity (spawning aggre- data on small-scale three-dimensional movement pat- gations) and changes in environmental conditions (i.e., terns of juvenile Atlantic tarpon (n = 4) by way of pas- temperature, dissolved oxygen) [6, 13, 15, 16, 39–41]. sive acoustic telemetry. The data can serve as a baseline We found that juvenile tarpon had distinct daytime for juvenile tarpon movement ecology that can further 50% KUDs, and core areas (0.07–0.20 km ) within be examined and use for comparison to adult move- Brewers Bay that overlapped very little with the other ments or other regions [6, 22]. Although most juvenile individuals for most of the year (< 2%). At night, tarpon tarpon (n = 8) left the bay shortly after tagging and their tended to move into or near a small, shallow lagoon in fate remained unknown, and two fish likely died or shed Brewers Bay, which resulted in an increase in overlap their tags, the remaining four fish provided useful data of 50% KUDs during most months. The spatial pat - on the movement ecology of juvenile tarpon. Juvenile terns displayed by juvenile tarpon suggest habitat par- tarpon were resident within the bay 78% to 99% of time, titioning during daytime and sheltering and protection but some transient behavior was observed for two of the from predation in a common area at night [6, 13, 17, larger individuals (i.e., both were 95 cm FL). One tarpon 18, 42]. During April, however, daytime overlap in 50% (ID #10979) left the bay for nearly 2 months (October KUD area showed a tenfold increase, as they shifted Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 10 of 14 Fig. 5 Water temperature (°C) and dissolved oxygen (mg/L) profiles for two locations in Brewers Bay: lagoon and airport runway (see Fig. 1) from February 1 to December 31, 2016. Red horizontal line indicated 30.5 °C temperature threshold in lagoon. Green (lagoon) and black (airport runway) horizontal line indicates location of juvenile tarpon (ID# 10979 and 10980) at night their activity space to similar areas within Brewers Bay. slower at night than other time periods, which suggests These changes in behavior and activity space coincided that juvenile tarpon were not feeding at this time. Fur- with the arrival of schools of bait fish as well as nesting ther research with improved experimental design will seabirds that feed on these schools in the spring [43, help to distinguish differences between adult and juve - 44]. When seabirds were present, we observed groups nile behavioral states such as resting, foraging or trave- of tarpon foraging on bait fish near the surface during ling [55]. the spring months primarily in the middle of Brewers Juvenile tarpon generally stayed less than 10  m Bay and near Black Point reef (Duffing Romero, M. and depth, but occasionally went to 25  m or deeper, which Nemeth, R.S., pers. observations). This feeding strategy is also typical for adult tarpon [6, 13]. Many coastal is not uncommon for tarpon and other pelagic preda- and pelagic fish, such as barracuda (Sphyraena barra - tors, which can increase their foraging success in the cuda), white marlin (Kajikia albida), dolphinfish (Cory - presence of seabirds feeding on bait fish at the water phaena. hippurus) and many species of tuna (Thunnus surface [15, 43, 45]. The areas of Brewers Bay where this spp) show similar vertical movement patterns, where feeding behavior was observed corresponded to April they spend the majority of time at shallow depths or daytime activity space of tagged tarpon. close to the surface and then make diel/seasonal deep Adult tarpon tend to feed at sunset and continue water movements [56–58]. Adult tarpon show a variety feeding into the night if there is enough food and avail- of vertical distributions that fall into four typical pat- able light for foraging [15, 46]. As with other species terns: (1) clear diel pattern shallow in day and deep at [47], ROM was assessed as a proxy for feeding. Simi- night; (2) deep in day and shallow at night; (3) deep and lar to adult tarpon, juveniles had the highest rates of shallow at irregular intervals throughout diel period, movement during dawn and dusk, which suggests and (4) random vertical movements throughout diel high feeding rates during crepuscular periods. How- period [6]. Juvenile tarpon in Brewers Bay showed a ever, this behavior may also indicate rapid movements consistent diel vertical movement pattern that matched along migration pathways between nighttime and day- pattern (2) where fish stayed shallow at night and time activity spaces [18, 48–54]. ROM was significantly deeper during the day. At smaller sizes juvenile tarpon D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 11 of 14 Fig. 6 Day and night relationships between average number of tarpon detections and a water temperature (°C) and b dissolved oxygen (mg/L) within the lagoon and along the airport runway Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 12 of 14 may select shallow, sheltered lagoon-type habitats, if with both acoustic and satellite tags and place additional available, as a strategy against predation [14, 15]. In this receivers along the coastlines or use a regional network study, all four tarpon used the Brewers Bay lagoon con- within and among neighboring islands [9, 40, 61, 62]. sistently throughout most of the year. Environmental conditions influenced tarpon behavior Abbreviations in Brewers Bay. Tarpon prefer water temperatures from COA: Center of activity; MCP: Minimum convex polygon; KUD: Kernel utiliza- 24 to 26  °C in spring and fall and 28–30  °C in summer tion distribution; ROM: Rate of movement; HR: Home range. [6, 13, 23]. We found that juvenile tarpon avoided water temperatures greater than 30  °C. For instance, tarpon Supplementary Information detection frequencies within the lagoon decreased at The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s40317- 021- 00239-x. temperatures above 29 °C and they did not enter nor rest in the lagoon at night when water temperature was higher Additional file 1: Table S1. Summary data for vertical distribution (m) of than 30.5  °C, but instead moved to deeper water on the juvenile tarpon from box plot analysis. south side of airport runway (Fig.  5). At this threshold temperature, tarpon faced a trade-off of remaining in Acknowledgements higher temperatures within the protected lagoon or leav- We want to thank Damon Bo Green and Tyler S. Best for assisting in the field ing the lagoon for cooler, less protected waters around to catch and tag many of the tarpon in this study. We thank Jonathan Jossart the airport runway at night. Previous studies on barra- for conducting detection range tests and assisting in the maintenance of the Brewers Bay acoustic array in the beginning of the project. We thank master’s cuda and bonefish (Albula vulpes ) have shown that both students in Marine and Environmental Studies who helped download acoustic species move to deeper waters away from their home receiver data in the field. We also want to thank the Center of Marine and range to avoid seasonal weather patterns and associ- Environmental Science at the University of the Virgin Islands for providing the facilities to complete this project. This is contribution # 212 of the University of ated temperature fluctuations [15, 39, 59]. Adult tarpon the Virgin Islands, Center for Marine and Environmental Studies. in Florida migrated farther northward on a daily basis as sea surface temperatures increased and seemed to track Authors’ contributions MDDR conducted most of the field work, data analyses/interpretation and the 26  °C isotherm from the Florida Keys to the south- writing; JKM contributed to data management/analyses; RSN secured funding ern coast of Virginia from May to July, respectively [6]. for project and contributed to field work; JL, SJP, JKM, JSA and RSN contrib - Despite the effect of high water temperatures on tarpon uted to data interpretation and writing of manuscript. All authors read and approved the final manuscript. behavior, tarpon tolerated low dissolved oxygen concen- trations in the lagoon, which is attributed to being facul- Funding tative air-breathers [13, 60]. Funding for this research was supported by VI-Established Program to Stimu- late Competitive Research ( VI-EPSCoR) through the NSF Grant #1355437. Conclusion Availability of data and materials To our knowledge, this acoustic telemetry study provided The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. some of the first information on juvenile tarpon move - ment ecology including home range size, rates of move- Declarations ment, vertical distribution, and habitat partitioning. Although limited to only four fish, our results showed Ethics approval and consent to participate high residency within a small bay and relatively stable All capture and tagging methodology on all fish in Brewers Bay was approved by the University of the Virgin Islands Institutional Animal Care and Use Com- non-overlapping daytime home ranges, except when sea- mittee (IRB #747807-1). sonally abundant food sources were present. Fine-scale acoustic tracking over multiple years showed the effects Consent for publication Not applicable. of changing environmental conditions on juvenile tarpon movement and habitat use. These baseline observations Competing interests highlight the need for more extensive studies of juvenile The authors declare that they have no competing interests. tarpon across a broader range of their distribution. In Author details addition to a larger sample size, we suggest including a 1 Center for Marine and Environmental Studies, University of the Virgin Islands, wider range of tarpon size classes, from small juveniles to 2 John Brewers, US Virgin Islands, St. Thomas 00803, USA. Great Lakes Institute for Environmental Research, University of Windsor, 2990 Riverside Dr. W, Wind- large reproductive adults, in future studies. Since tarpon sor, ON N9C 1A2, Canada. Department of Marine Ecosystems and Society, are highly mobile but also show resident behavior [6, 7, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA. 13, 40], it is difficult to assess their larger-scale movement Marine Conservation Research Group, School of Biological and Marine Sci- ences, Marine Building, University of Plymouth, Plymouth PL4 8AA, UK. patterns using an acoustic array limited to one bay. A bet- ter approach, to facilitate tracking tarpon movements Received: 24 July 2020 Accepted: 7 April 2021 over a broader geographic range, would be to tag tarpon D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 13 of 14 References 20. Crabtree RE, Snodgrass D, Harnden C. Maturation and reproductive 1. Pittman SJ, McAlpine CA. Movements of marine fish and decapod seasonality in bonefish, Albula vulpes, from the waters of the Florida Keys. crustaceans: process, theory and application. In: Advances in marine biol- Fishery Bulletin. 3:10. Available from: https:// spo. nmfs. noaa. gov/ conte nt/ ogy. Elsevier; 2003. pp. 205–94. https:// doi. org/ 10. 1016/ S0065- 2881(03) matur ation- and- repro ducti ve- seaso nality- bone fish- albula- vulpes- waters- 44004-2.flori da- keys . Accessed Mar 2016. 2. Dingle H, Drake VA. What is migration? BioScience. 2007;57:113–21. 21. Baldwin J, Snodgrass D. 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Movement patterns of juvenile Atlantic tarpon (Megalops atlanticus) in Brewers Bay, St. Thomas, U.S. Virgin Islands

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Abstract

Background: Atlantic tarpon (Megalops atlanticus) are a highly migratory species ranging along continental and insular coastlines of the Atlantic Ocean. Due to their importance to regional recreational and sport fisheries, research has been focused on large-scale movement patterns of reproductively active adults in areas where they are of high economic value. As a consequence, geographically restricted focus on adults has left significant gaps in our under - standing of tarpon biology and their movements, especially for juveniles in remote locations where they are common. Our study focused on small-scale patterns of movement and habitat use of juvenile tarpon using acoustic telemetry in a small bay in St. Thomas, US Virgin Islands. Results: Four juvenile tarpon (80–95 cm FL) were tracked from September 2015 to February 2018, while an addi- tional eight juveniles (61–94 cm FL) left the study area within 2 days after tagging and were not included in analysis. 2 2 Four tarpon had > 78% residency and average activity space of 0.76 km (range 0.08–1.17 km ) within Brewers Bay (1.8 km ). Their vertical distribution was < 18 m depth with occasional movements to deeper water. Activity was greater during day compared to night, with peaks during crepuscular periods. During the day tarpon used different parts of the bay with consistent overlap around the St. Thomas airport runway and at night tarpon typically remained in a small shallow lagoon. However, when temperatures in the lagoon exceeded 30 °C, tarpon moved to cooler, deeper waters outside the lagoon. Conclusion: Our results, although limited to only four individuals, provide new baseline data on the movement ecol- ogy of juvenile Atlantic tarpon. We showed that juvenile tarpon had high residency within a small bay and relatively stable non-overlapping daytime home ranges, except when seasonally abundant food sources were present. Fine- scale acoustic tracking showed the effects of environmental conditions (i.e., elevated seawater temperature) on tar - pon movement and habitat use. These observations highlight the need for more extensive studies of juvenile tarpon across a broader range of their distribution, and compare the similarities and differences in behavior among various size classes of individuals from small juveniles to reproductively mature adults. Keywords: Acoustic telemetry, Home range, Vertical movement, Diel movement, Environmental effects Background Tracking the movements and migrations of animals in the aquatic environment provides insight into spatial and tem- *Correspondence: marapp15@gmail.com poral patterns of habitat use, trophic interactions, reproduc- Center for Marine and Environmental Studies, University of the Virgin tive behavior, and behavioral responses to environmental Islands, 2 John Brewers, US Virgin Islands, St. Thomas 00803, USA Full list of author information is available at the end of the article change [1–7]. Recent studies have shown that some highly © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 2 of 14 migratory species can exhibit high site fidelity to discrete mostly soft muddy bottom with scattered rocks and dead nearshore areas between migratory events, whereas rela- corals. It is partly enclosed by the airport runway with tively site-attached species can undergo repeated large-scale the remaining shoreline composed of rocky reef or soft migrations for reproduction [1, 8–10]. Integrating these sediments, and red mangroves (Rhizophora mangle). variable patterns of large-scale movements and small-scale activity spaces are becoming increasingly important for Acoustic array implementing ecosystem-based fisheries management, The acoustic monitoring system consisted of 45 omnidi - understanding connectivity, and designing ecologically rel- rectional receivers (VR2W, 69  kHz, Innovasea Systems evant marine managed areas [5, 11, 12]. Inc. (previously Vemco), Halifax, Nova Scotia, Canada) Atlantic tarpon (Megalops atlanticus) is a highly mobile that were moored, and spaced equally across Brewers Bay, pelagic species that supports important recreational and including eastern Perseverance Bay, and along the southern sport fisheries. Tarpon range across coastal areas, estuaries, side of the airport runway (Fig. 1). Range testing of receiv- and rivers of the western and eastern Atlantic Ocean, the ers [24] across the study site was conducted over four days Caribbean Islands, and the Gulf of Mexico [6, 13, 14]. Tar- in June 2015, by placing receivers in depths ranging from pon spend their larval stage as leptocephali in open ocean, 5 to 19  m over different substrate types including shallow and as juveniles settle nearshore in tropical and subtropi- and deep coral/rock and seagrass/sand [25]. Probabilities cal estuarine, mangrove and lagoon habitats, where food of transmission were tested using three A69-1601 Inno- resources are high and predator pressures are low [15–18]. vaSea transmitters V9-2H (151  dB), V13-1H (153  dB) and Adult tarpon range in size from 90–250  cm fork length V16-4H (158  dB) that transmitted every 60  s. Transmit- (FL) and males reach sexual maturity at about 90 cm while ters were attached to mooring lines, connected to cinder females at 128 cm FL [13, 19–21]. Much of our knowledge blocks, and suspended 1 m above the bottom. A detection of tarpon movements and behaviors come from satellite probability of 70% for V13-1H transmitters was selected tracking and conventional anchor tag studies conducted in providing high coverage throughout the study area with Florida, southeast Atlantic, Gulf of Mexico, and the north- estimated detection ranges of 101  m in seagrass/sand and western Caribbean (e.g., Mexico, Belize, Cuba) [6, 7, 13, 14, 120 m in coral/rock substrates (Fig.  1). Seawater tempera- 22, 23]. These studies have focused on large-scale move - ture and dissolved oxygen (DO) were collected at several ments (> 500 km) of large adult tarpon (> 130 cm FL) that stations in Brewers Bay using Hobo temperature loggers support a valuable sport fishery. The focus on adult tarpon (Onset Computer Corporation, Bourne, MA, USA) and over a limited geographic range leaves large gaps in our miniDot DO loggers (Precision Measurement Engineering understanding of tarpon biology and movement ecology, Inc, Vista, CA, USA) that were attached to acoustic receiver especially in insular areas throughout the eastern Carib- moorings. Temperature loggers were deployed in August bean where they are common [13]. We applied acoustic 2015, DO loggers were deployed in February 2016, and telemetry to quantify activity space, rates of movement, both recorded data at 15-min intervals (Fig. 1). vertical distribution and habitat use of juvenile tarpon across diel and seasonal time scales. Additionally, we exam- Fish capture ined how environmental conditions (i.e., water tempera- All capture and tagging methodology in Brewers Bay was ture, dissolved oxygen) influenced their behavior. approved by the University of the Virgin Islands Institu- tional Animal Care and Use Committee (IRB #747807- Materials and methods 1). Juvenile Atlantic tarpon were caught using hook and Study site line from a boat or dock between September 2015 and Brewers Bay is located on the western end of St. Thomas, November 2016. As each fish was reeled in, it was guided U.S. Virgin Islands (18°20′28″N, 64°58′40″W) and is alongside the boat or dock and into a floating cradle bounded by a commercial airport runway and small constructed of PVC pipe, plastic mesh, and foam noo- lagoon on the south, a sandy beach on the north-east- dles for buoyancy. Once in the cradle, the fish was held ern shore, and a rocky headland and smaller bay (Per- under water, turned upside-down to induce tonic-immo- severance Bay) to the northwest (Fig.  1). Brewers Bay is bility, and the hook was removed from the mouth. Each 1.8 km in area, ranges in depth between 0 and 33.1  m fish ( n = 14) was measured for fork length (FL) and total (Fig.  1), and has steep vertical slopes along the airport length (TL) to the nearest millimeter (mm). Acoustic runway and around the rocky headland. The bay is com - transmitters (either V13 [13 mm × 36 mm; n = 8] or V13P posed of a variety of habitat types including sand, sea- [13 mm × 46  mm; n = 6; pressure tags that provide depth grass, patch reefs, fringing coral reefs, rocky reefs, and data], 69 kHz, Innovasea Inc, Halifax, NS, Canada) were rubble and reinforced concrete blocks (dolosse) around surgically implanted into the body cavity on the ventral the seaward slopes of the airport runway. The lagoon is side of the fish [26]. The incision was closed with surgical D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 3 of 14 Fig. 1 Map of the Caribbean (a) and the island of St. Thomas in the US Virgin Islands (b) and study site in Brewers Bay (c) depicting bathymetry and the acoustic array with station number and approximate range of 70% detection probability (circles). Detection ranges varied by habitat (deep hard bottom = 115 m, deep soft bottom = 120 m, shallow soft and hard bottom = 101 m) based on range testing. Location of environmental data logger stations shown as green dots (temperature) and red diamonds (dissolved oxygen). Yellow dots represent approximate location where juvenile Atlantic tarpon were tagged and released. Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 4 of 14 staples and treated with antibacterial ointment (note: Temporal data were examined for seasonal and diel pat- antibacterial ointment is no longer used on incision and terns. Seasons were defined as spring (March, April, May), sutures). Fish remained immersed in open seawater the summer (June, July, August), fall (September, October, entire time so no general or local anesthetic was admin- November) and winter (December, January, February). istered, which allowed for the release of fish shortly after Crepuscular periods were calculated using astronomi- tagging and data collection were completed. Fish were cal twilight based on daily sunrise/sunset  time charts for turned back over, the head was faced into the current to Charlotte Amalie, St. Thomas, U. S. Virgin Islands [28]. increase ventilation, and after a few minutes of recovery, Specifically, dawn was defined as − 1 h before astronomi- fish were released at the capture location (Fig. 1). cal morning and + 1 h after sunrise to account for seasonal changes in day length. Likewise, dusk was defined as  − 1 h Data processing before astronomical twilight to + 1 h after sunset. Day and Detections were downloaded from receivers every 3 night periods were the remaining  hours between brack- months and analyzed using R Version 3.4.3 [27]. For each eted dawn and dusk, respectively. tarpon (n = 14) the total number of detections, first/last day detected, number of days between first and last day, and total days detected were calculated. Detections for Data analysis and statistics each individual tarpon by receiver were plotted through Residency index was calculated for the four fish used in time to investigate the presence of dropped tags, dead indi- analyses by dividing total days each fish was detected viduals, and short-term residency. Of the 14 juvenile tar- within the Brewers Bay array by number of days between pon that were tagged, four (n = 4) individuals had at least the first and last detection. Residency Index was defined 1  month of tracking data to conduct spatial home range as the percentage of days spent within Brewers Bay array analysis. Three of these tarpon were detected for 344–472 for the duration of time that each fish was tracked. days and also had pressure transmitters, thus were used Center of activity (COA) for juvenile tarpon (n = 4) was to analyze monthly and seasonal trends in rates of move- calculated every 30  min using mean position (latitude ment, activity space, and vertical distribution (Table 1). Of and longitude) of all detections during that time step [29]. the remaining ten tarpon that were excluded from analy- Distance between COA relocation points and difference sis, eight (n = 8) were within the array two days or less and in time between each relocation point were calculated had insufficient detections for analyses, and two (n = 2) for each fish using ‘adehabitatLT’ package of R environ - had either died or shed their tags (Table 1). ment [30]. COA values were used to calculate rate of Table 1 Summary data for Atlantic tarpon (M. atlanticus) caught and tracked in Brewers Bay acoustic array, including date caught (mm/dd/yyyy), total length ( TL), fork length (FL), total number of detections and total residency time detected in Brewers Bay Fish ID Tag date TL (cm) FL (cm) Total First day Last day Days between Total days Residency detections detected detected first and last detected index (%) detection 36032 9/17/2015 109 95 12231 9/17/2015 10/19/2015 32 28 88 10980P 6/17/2016 96 80 54564 6/18/2016 5/28/2017 344 330 96 10979P 6/26/2016 112 95 106564 6/26/2016 7/1/2017 370 287 78 2966P 10/25/2016 96 85 395606 10/26/2016 2/10/2018 472 464 99 36034 10/16/2015 90 78 326110 10/16/2015 7/11/2016 269 271 n/a 36036 10/21/2015 130 91.2 2017 10/22/2015 1/25/2016 95 74 n/a 59272 1/12/2016 86.4 76.1 10 1/12/2016 1/13/2016 1 1 n/a 36044 5/24/2016 70 61 5 5/24/2016 5/24/2016 1 1 n/a 36045 6/1/2016 130 91.2 14 6/1/2016 6/1/2016 1 1 n/a 2965P 8/8/2016 96 85 70 8/9/2016 8/9/2016 1 1 n/a 2964P 8/14/2016 100 80 11 8/14/2016 8/14/2016 1 1 n/a 36039 8/16/2016 100 94 10 8/16/2016 8/16/2016 1 1 n/a 2963P 9/15/2016 92 77 660 9/16/2016 9/17/2016 2 2 n/a 24976 10/29/2016 96 83 212 11/8/2016 11/8/2016 1 1 n/a P acoustic pressure transmitter measured depth, n/a not applicable Fish used for Brewers Bay spatial analyses Transient fish not used in spatial analyses Fish died or shed tag D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 5 of 14 movement (ROM) and activity space for individual fish, points. Kruskal–Wallis and Tukey post hoc tests were and included minimum convex polygons (100% MCP) used to test for differences in ROM between diel periods and kernel utilization distributions (50% and 95% KUD). and a two-way ANOVA was used to test for differences in Activity space, which incorporates MCP, 50% KUD and diel ROM across seasons. ROM provides a useful metric 95% KUD, was calculated using the ‘move’ and ‘adehabi- for fish activity during diel periods and can also be used tat’ package in R environment [30, 31]. MCPs provided as a proxy for feeding behavior [47]. information on the extent of an individual’s range or Vertical distribution was calculated for tarpon tagged area used and included all outlying points that might be with depth-enabled transmitters (n = 3, Table  1). Depth the result of exploratory movement or periodic migra- measurements were binned into hourly and monthly tion not part of their typical activity. KUDs highlight the periods and boxplots were applied to elucidate their ver- density of positions of an individual within the activity tical movement patterns. ANOVA and Tukey post hoc space based on COAs (i.e., 50% KUD = high density, 95% tests were used to test for differences in vertical move - KUD = low density), as well as estimated error around ment across diel and monthly periods. these positions [32, 33]. When necessary, a ‘land’ barrier Environmental conditions and their relationship to polygon was used to clip out the area of MCP and KUD tarpon movement and habitat use were assessed for sea- polygons that fell on land (‘rgeos’ package, [34]). The cal - water temperature and DO. Daily average number of culated MCP and KUD (50% and 95%) activity spaces detections, average temperature and average DO within were plotted in ArcGIS 10.6 for annual, monthly, and diel the lagoon and waters along the airport runway were periods. To calculate the degree of overlap in 50% and analyzed by applying a linear regression for the study 95% KUD among individuals over diel and monthly time period (September 2015—February 2018). periods, a home range (HR) percent overlap analyses was applied using the ‘kerneloverlaphr’ function of the ‘ade- Results habitatHR’ package [30, 35, 36]. The HR percent overlap Fourteen (n = 14) juvenile tarpon were captured and analyses calculates the proportion of animal a’s home acoustically tagged in Brewers Bay (average FL 83.7  cm, range that is overlapped by animal b’s home range [30, 35, range 61–95 cm; Table 1). Only four (n = 4) juvenile tarpon 36]. The data output matrix provides indices of overlap provided a sufficient number of detections over a sufficient for all pairs of animals [35, 36]. Using the matrix output, duration (32–472 days), and a residency index of 78–100%, average and ranges in fish overlap values were calculated. to be included in our spatial analysis (Table 1). Eight (n = 8) Repeated measures analyses of variance (RM-ANOVA) s fi h were detected for less than a week and had fewer than was used to test for differences in KUD across monthly 1000 detections and upon assessment, it was determined and diel periods. All monthly analyses used data from that the two remaining fish detected within the bay had three (n = 3) tarpon that had average KUD activity space died or shed their tags within one day following release. representing each month (Table  1). Individual tarpon were treated as random variables, and either monthly Activity space or diel periods were treated for autocorrelation effects The activity space of juvenile tarpon varied among indi - (‘corAR1’) using the ‘lme’ function of the ‘nlme’ package viduals and through time. The average MCP for juve - for R [37, 38]. To assess relationship between monthly 2 2 nile tarpon (n = 4) was 0.97 k m (range 0.77–1.17 k m ), ROM and 50% KUD size, a linear regression was applied. 2 while the average 95% and 50% KUD was 0.76 km (range Rate of movement (ROM, m/s) was calculated by divid- 2 2 2 0.49–0.99 km ) and 0.13 k m (range 0.08–0.20 k m ), ing the distance between consecutive COA position val- respectively (Table  2; Fig.  2). Comparison of mean day, ues by the time difference between these consecutive Table 2 Calculated home range size (km ) for each tarpon based on 50% and 95% Kernel utilization distribution (KUD) and 100% minimum convex polygon (MCP); number of center of activity (COA) points that fell on land and total percentage of COA points on land removed out of total COA points used for home range analyses Fish ID Total COA points MCP 100% area KUD 95% area KUD 50% area COA points on Percentage 2 2 2 (km ) (km ) (km ) land of COA points removed 2966 19,367 1.174 0.988 0.200 123 0.64 10979 11,888 1.055 0.619 0.075 163 1.37 10980 10,425 0.864 0.492 0.090 166 1.59 36032 887 0.767 0.938 0.149 7 0.79 In this case 100% MCP is smaller than 95% KUD based on how they are calculated (see “Materials and methods”) Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 6 of 14 Fig. 2 Activity space of juvenile tarpon (n = 4) based on yearlong 100 % MCP (black line in left panels), and 50% and 95% KUD for day (yellow/ orange left panels), night (blue/green right panels), and crepuscular (dawn = red, dusk = blue middle panels) time periods. The arrow represents an example of a corridor between day and night activity space. See Fig. 1 for labels. D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 7 of 14 Table 3 Summary of 50% and 95% Kernel utilization distribution (KUD) overlap for juvenile tarpon (n = 3) during day and night for full year, May to March (April excluded) and only April Month(s) Diel period KUD 50% area ± SE KUD 50% area range KUD 95% area ± SE KUD 95% area 2 2 2 2 (km ) (km ) (%) (km )range (km ) (%) All year Day 12% ± 6% 0–27 42% ± 12% 11–72 All year Night 20% ± 18% 0–99 51% ± 8% 28–99 May–March Day 2% ± 2% 0–6 23% ± 14% 8–55 May–March Night 19% ± 18% 0–99 44% ± 10% 14–99 April Day 20% ± 16% 1–55 63% ± 4% 42–74 April Night 10% ± 9% 0–32 33% ± 19% 11–81 night and crepuscular activity spaces among juvenile tar- 05:00 and at 18:00 (Fig.  3a). ROM was not significantly pon for both 50% and 95% KUDs were not significantly different across months (mean = 0.07 m/s ± 0.01 SD), but different across diel and crepuscular periods (50% KUD: there was a strong relationship between monthly ROM p = 0.07; 95% KUD: p = 0.44) and across months (50% and 50% KUD (F = 34.07, P = 0.0001, R = 0.77) with the KUD: p = 0.78; 95% KUD: p = 0.29). highest rates for both metrics during the months of April, Analysis of daytime activity space overlap averaged June and September (Fig. 3b). 12% for 50% KUD and 42% for 95% KUD during the year (Table  3), with each tarpon showing distinct 50% KUD Vertical movement core areas centered around northwest corner of runway Vertical movement of juvenile tarpon with pressure trans- (ID#36032), around Black Point and deeper part of Brew- mitters (n = 3) varied among time of the day (ANOVA: ers Bay (ID#2966), in and around the lagoon and Range F = 36,526, P < 0.0001) (Fig. 4). Tarpon used more of the 1,3 Cay extending to shallow and deep parts of Brewers Bay water column during the day ranging between 2 to 13 m (ID#10979), and around the tip of runway (ID#10980) average depth and 16 to 27  m maximum depth (Fig.  4). (Fig.  2, day). In April, however, overlap for 50% and 95% At night, tarpon stayed in shallower waters ranging from KUD during daytime showed an increase to 20% and 0 to 5  m average depth and 8 to 14  m maximum depth 63%, respectively (Table 3). Excluding the month of April, (Fig.  4; Additional file  1: Table  S1). Nighttime vertical daytime 50% and 95% KUD overlap values declined from movements were partly constrained when tarpon were in 12 to 2% and 42% to 23%, respectively (Table 3). At night- lagoon (maximum depth 4  m, Fig.  2). During dawn and time, 50% KUD areas were centered in shallow Brewers dusk, average depth of tarpon ranged between 0 to 8  m Bay, around the airport runway and particularly inside (Fig.  4; Additional file  1: Table  S1). Vertical distribution the shallow lagoon, where juvenile tarpon went at night across months showed no consistent patterns among the (Fig.  2, night). Consistent use of these areas at night three tarpon with depth transmitters. tended to increase nighttime 50% and 95% KUD overlap relative to daytime, except for April, when space overlap Movement and environmental variability decreased at night (Table 3). Water temperature in Brewers Bay ranged from 25–28 °C in winter to 29–32  °C in late summer and early fall. Rate of movement Inside the lagoon water temperature showed greater Average ROM of juvenile tarpon was 0.07  m/s fluctuations on a daily basis and had a greater range (± 0.02 SD) and was significantly different among (mean = 28.3  °C ± 1.27 SD, range = 24.8–32.0 °C) than in diel periods (H = 12.4, P < 0.006). Post hoc com- the bay (mean = 28.1  °C ± 1.15 SD, range = 25.6–30.6  °C) parisons between day (mean = 0.06  m/s ± 0.01 (Fig.  5). Water temperature had a strong effect on tar - SD), night (mean = 0.05  m/s ± 0.01 SD), pon movement and habitat use. We found a significant dawn (mean = 0.09  m/s ± 0.01 SD) and dusk negative relationship between number of tarpon detec- (mean = 0.10  m/s ± 0.01 SD) showed a significant differ - tions and temperature in the lagoon at night (adjusted ence between dusk and nighttime periods only (Tukey R = 0.0.32; P < 0.001), but no relationship between fre- HSD: P < 0.01). Diel ROM also varied across seasons quency of detections in the lagoon or around the runway (2-way ANOVA: F = 253.2, P < 0.0001). Most notable, at other times of day (Fig. 6). Juvenile tarpon were present 1,15 daytime ROM was significantly lower in winter com - in the lagoon at night when temperature ranged between pared to other seasons (Tukey HSD: P < 0.001). During 26 and 28  °C; however, once temperature reached 29  °C all seasons, crepuscular ROM peaked between 04:00 to frequency of tarpon detections decreased rapidly and Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 8 of 14 Fig. 3 a Diel ROM of juvenile tarpon by season of the year: Spring (March, April, May), Summer (June, July, August), Fall (September, October, November) and Winter (December, January, February). b Relationship between average ROM and core activity space 50% KUD for four juvenile tarpon during each month stopped at about 30.5  °C (Fig.  6), indicating tarpon left 249, 285, 251, 282; Fig.  1), where nighttime maximum the lagoon. Water temperatures in the lagoon reached or water temperatures were cooler (Figs. 5, 6a). When water exceeded 30.5 °C on 59 day of the study period compared temperatures in lagoon cooled to below 30.5 °C, juvenile to only 4 days at the airport runway. Likewise, water tem- tarpon returned to resting in lagoon at night (Fig. 5). peratures 26  °C colder were recorded on 61 day in the Similar to water temperature, dissolved oxygen concen- lagoon but only on 16 day along runway. At times of high trations in the lagoon varied widely from 0.9 to 7.1 mg/L lagoon temperatures, juvenile tarpon left the lagoon and (mean = 4.7 ± 1.89 SD), but were more stable along had higher frequency of detections at night along the tip the airport runway (mean = 6.1 ± 1.9 SD, range 5.3– and south side of the airport runway (i.e., stations 248, 6.6 mg/L) (Fig.  5). Based on detection frequencies, there D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 9 of 14 Fig. 4 Boxplot of daily distributions by hour of vertical movement of three juvenile tarpon during diel (day, night) and crepuscular (dawn, dusk) periods was no significant relationship in number of detections and November) before returning to its home range of tarpon at different levels of dissolved oxygen within for another 7  months. The second tarpon (ID#3032) the lagoon or the runway (Fig. 6b), indicating that tarpon remained within Brewers Bay for 1 month before depart- seemed to tolerate the low oxygen levels in the lagoon, ing mid-October, but it was then detected at an acoustic especially at night array 12  km offshore in January. Interestingly, both tar - pon departed in October when water temperature was high. Seasonal movements, such as these, by Atlantic Discussion tarpon and other coastal species have been attributed to To our knowledge, this study provided some of the first food availability, reproductive maturity (spawning aggre- data on small-scale three-dimensional movement pat- gations) and changes in environmental conditions (i.e., terns of juvenile Atlantic tarpon (n = 4) by way of pas- temperature, dissolved oxygen) [6, 13, 15, 16, 39–41]. sive acoustic telemetry. The data can serve as a baseline We found that juvenile tarpon had distinct daytime for juvenile tarpon movement ecology that can further 50% KUDs, and core areas (0.07–0.20 km ) within be examined and use for comparison to adult move- Brewers Bay that overlapped very little with the other ments or other regions [6, 22]. Although most juvenile individuals for most of the year (< 2%). At night, tarpon tarpon (n = 8) left the bay shortly after tagging and their tended to move into or near a small, shallow lagoon in fate remained unknown, and two fish likely died or shed Brewers Bay, which resulted in an increase in overlap their tags, the remaining four fish provided useful data of 50% KUDs during most months. The spatial pat - on the movement ecology of juvenile tarpon. Juvenile terns displayed by juvenile tarpon suggest habitat par- tarpon were resident within the bay 78% to 99% of time, titioning during daytime and sheltering and protection but some transient behavior was observed for two of the from predation in a common area at night [6, 13, 17, larger individuals (i.e., both were 95 cm FL). One tarpon 18, 42]. During April, however, daytime overlap in 50% (ID #10979) left the bay for nearly 2 months (October KUD area showed a tenfold increase, as they shifted Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 10 of 14 Fig. 5 Water temperature (°C) and dissolved oxygen (mg/L) profiles for two locations in Brewers Bay: lagoon and airport runway (see Fig. 1) from February 1 to December 31, 2016. Red horizontal line indicated 30.5 °C temperature threshold in lagoon. Green (lagoon) and black (airport runway) horizontal line indicates location of juvenile tarpon (ID# 10979 and 10980) at night their activity space to similar areas within Brewers Bay. slower at night than other time periods, which suggests These changes in behavior and activity space coincided that juvenile tarpon were not feeding at this time. Fur- with the arrival of schools of bait fish as well as nesting ther research with improved experimental design will seabirds that feed on these schools in the spring [43, help to distinguish differences between adult and juve - 44]. When seabirds were present, we observed groups nile behavioral states such as resting, foraging or trave- of tarpon foraging on bait fish near the surface during ling [55]. the spring months primarily in the middle of Brewers Juvenile tarpon generally stayed less than 10  m Bay and near Black Point reef (Duffing Romero, M. and depth, but occasionally went to 25  m or deeper, which Nemeth, R.S., pers. observations). This feeding strategy is also typical for adult tarpon [6, 13]. Many coastal is not uncommon for tarpon and other pelagic preda- and pelagic fish, such as barracuda (Sphyraena barra - tors, which can increase their foraging success in the cuda), white marlin (Kajikia albida), dolphinfish (Cory - presence of seabirds feeding on bait fish at the water phaena. hippurus) and many species of tuna (Thunnus surface [15, 43, 45]. The areas of Brewers Bay where this spp) show similar vertical movement patterns, where feeding behavior was observed corresponded to April they spend the majority of time at shallow depths or daytime activity space of tagged tarpon. close to the surface and then make diel/seasonal deep Adult tarpon tend to feed at sunset and continue water movements [56–58]. Adult tarpon show a variety feeding into the night if there is enough food and avail- of vertical distributions that fall into four typical pat- able light for foraging [15, 46]. As with other species terns: (1) clear diel pattern shallow in day and deep at [47], ROM was assessed as a proxy for feeding. Simi- night; (2) deep in day and shallow at night; (3) deep and lar to adult tarpon, juveniles had the highest rates of shallow at irregular intervals throughout diel period, movement during dawn and dusk, which suggests and (4) random vertical movements throughout diel high feeding rates during crepuscular periods. How- period [6]. Juvenile tarpon in Brewers Bay showed a ever, this behavior may also indicate rapid movements consistent diel vertical movement pattern that matched along migration pathways between nighttime and day- pattern (2) where fish stayed shallow at night and time activity spaces [18, 48–54]. ROM was significantly deeper during the day. At smaller sizes juvenile tarpon D uffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 11 of 14 Fig. 6 Day and night relationships between average number of tarpon detections and a water temperature (°C) and b dissolved oxygen (mg/L) within the lagoon and along the airport runway Duffing Romero et al. Anim Biotelemetry (2021) 9:16 Page 12 of 14 may select shallow, sheltered lagoon-type habitats, if with both acoustic and satellite tags and place additional available, as a strategy against predation [14, 15]. In this receivers along the coastlines or use a regional network study, all four tarpon used the Brewers Bay lagoon con- within and among neighboring islands [9, 40, 61, 62]. sistently throughout most of the year. Environmental conditions influenced tarpon behavior Abbreviations in Brewers Bay. Tarpon prefer water temperatures from COA: Center of activity; MCP: Minimum convex polygon; KUD: Kernel utiliza- 24 to 26  °C in spring and fall and 28–30  °C in summer tion distribution; ROM: Rate of movement; HR: Home range. [6, 13, 23]. We found that juvenile tarpon avoided water temperatures greater than 30  °C. For instance, tarpon Supplementary Information detection frequencies within the lagoon decreased at The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s40317- 021- 00239-x. temperatures above 29 °C and they did not enter nor rest in the lagoon at night when water temperature was higher Additional file 1: Table S1. Summary data for vertical distribution (m) of than 30.5  °C, but instead moved to deeper water on the juvenile tarpon from box plot analysis. south side of airport runway (Fig.  5). At this threshold temperature, tarpon faced a trade-off of remaining in Acknowledgements higher temperatures within the protected lagoon or leav- We want to thank Damon Bo Green and Tyler S. Best for assisting in the field ing the lagoon for cooler, less protected waters around to catch and tag many of the tarpon in this study. We thank Jonathan Jossart the airport runway at night. Previous studies on barra- for conducting detection range tests and assisting in the maintenance of the Brewers Bay acoustic array in the beginning of the project. We thank master’s cuda and bonefish (Albula vulpes ) have shown that both students in Marine and Environmental Studies who helped download acoustic species move to deeper waters away from their home receiver data in the field. We also want to thank the Center of Marine and range to avoid seasonal weather patterns and associ- Environmental Science at the University of the Virgin Islands for providing the facilities to complete this project. This is contribution # 212 of the University of ated temperature fluctuations [15, 39, 59]. Adult tarpon the Virgin Islands, Center for Marine and Environmental Studies. in Florida migrated farther northward on a daily basis as sea surface temperatures increased and seemed to track Authors’ contributions MDDR conducted most of the field work, data analyses/interpretation and the 26  °C isotherm from the Florida Keys to the south- writing; JKM contributed to data management/analyses; RSN secured funding ern coast of Virginia from May to July, respectively [6]. for project and contributed to field work; JL, SJP, JKM, JSA and RSN contrib - Despite the effect of high water temperatures on tarpon uted to data interpretation and writing of manuscript. All authors read and approved the final manuscript. behavior, tarpon tolerated low dissolved oxygen concen- trations in the lagoon, which is attributed to being facul- Funding tative air-breathers [13, 60]. Funding for this research was supported by VI-Established Program to Stimu- late Competitive Research ( VI-EPSCoR) through the NSF Grant #1355437. Conclusion Availability of data and materials To our knowledge, this acoustic telemetry study provided The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. some of the first information on juvenile tarpon move - ment ecology including home range size, rates of move- Declarations ment, vertical distribution, and habitat partitioning. Although limited to only four fish, our results showed Ethics approval and consent to participate high residency within a small bay and relatively stable All capture and tagging methodology on all fish in Brewers Bay was approved by the University of the Virgin Islands Institutional Animal Care and Use Com- non-overlapping daytime home ranges, except when sea- mittee (IRB #747807-1). sonally abundant food sources were present. Fine-scale acoustic tracking over multiple years showed the effects Consent for publication Not applicable. of changing environmental conditions on juvenile tarpon movement and habitat use. These baseline observations Competing interests highlight the need for more extensive studies of juvenile The authors declare that they have no competing interests. tarpon across a broader range of their distribution. In Author details addition to a larger sample size, we suggest including a 1 Center for Marine and Environmental Studies, University of the Virgin Islands, wider range of tarpon size classes, from small juveniles to 2 John Brewers, US Virgin Islands, St. Thomas 00803, USA. Great Lakes Institute for Environmental Research, University of Windsor, 2990 Riverside Dr. W, Wind- large reproductive adults, in future studies. Since tarpon sor, ON N9C 1A2, Canada. Department of Marine Ecosystems and Society, are highly mobile but also show resident behavior [6, 7, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA. 13, 40], it is difficult to assess their larger-scale movement Marine Conservation Research Group, School of Biological and Marine Sci- ences, Marine Building, University of Plymouth, Plymouth PL4 8AA, UK. patterns using an acoustic array limited to one bay. 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