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

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 understanding 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. Four juvenile tarpon (80–95 cm FL) were tracked from September 2015 to February 2018, while an additional eight juveniles (61–94 cm FL) left the study area within 2 days after tagging and were not included in analysis. Four tarpon had > 78% residency and average activity space of 0.76 km2 (range 0.08–1.17 km2) within Brewers Bay (1.8 km2). 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. Our results, although limited to only four individuals, provide new baseline data on the movement ecology 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 tarpon 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.


Background
Tracking the movements and migrations of animals in the aquatic environment provides insight into spatial and temporal patterns of habitat use, trophic interactions, reproductive behavior, and behavioral responses to environmental change [1][2][3][4][5][6][7]. Recent studies have shown that some highly

Open Access
Animal Biotelemetry *Correspondence: marapp15@gmail.com 1 Center for Marine and Environmental Studies, University of the Virgin Islands, 2 John Brewers, US Virgin Islands, St. Thomas 00803, USA Full list of author information is available at the end of the article migratory species can exhibit high site fidelity to discrete nearshore areas between migratory events, whereas relatively site-attached species can undergo repeated large-scale migrations for reproduction [1,[8][9][10]. Integrating these variable patterns of large-scale movements and small-scale activity spaces are becoming increasingly important for implementing ecosystem-based fisheries management, understanding connectivity, and designing ecologically relevant marine managed areas [5,11,12].
Atlantic tarpon (Megalops atlanticus) is a highly mobile pelagic species that supports important recreational and sport fisheries. Tarpon range across coastal areas, estuaries, and rivers of the western and eastern Atlantic Ocean, the Caribbean Islands, and the Gulf of Mexico [6,13,14]. Tarpon spend their larval stage as leptocephali in open ocean, and as juveniles settle nearshore in tropical and subtropical estuarine, mangrove and lagoon habitats, where food resources are high and predator pressures are low [15][16][17][18]. Adult tarpon range in size from 90-250 cm fork length (FL) and males reach sexual maturity at about 90 cm while females at 128 cm FL [13,[19][20][21]. Much of our knowledge of tarpon movements and behaviors come from satellite tracking and conventional anchor tag studies conducted in Florida, southeast Atlantic, Gulf of Mexico, and the northwestern Caribbean (e.g., Mexico, Belize, Cuba) [6,7,13,14,22,23]. These studies have focused on large-scale movements (> 500 km) of large adult tarpon (> 130 cm FL) that support a valuable sport fishery. The focus on adult tarpon over a limited geographic range leaves large gaps in our understanding of tarpon biology and movement ecology, especially in insular areas throughout the eastern Caribbean where they are common [13]. We applied acoustic telemetry to quantify activity space, rates of movement, vertical distribution and habitat use of juvenile tarpon across diel and seasonal time scales. Additionally, we examined how environmental conditions (i.e., water temperature, dissolved oxygen) influenced their behavior.

Study site
Brewers Bay is located on the western end of St. Thomas, U.S. Virgin Islands (18°20′28″N, 64°58′40″W) and is bounded by a commercial airport runway and small lagoon on the south, a sandy beach on the north-eastern shore, and a rocky headland and smaller bay (Perseverance Bay) to the northwest (Fig. 1). Brewers Bay is 1.8 km 2 in area, ranges in depth between 0 and 33.1 m (Fig. 1), and has steep vertical slopes along the airport runway and around the rocky headland. The bay is composed of a variety of habitat types including sand, seagrass, patch reefs, fringing coral reefs, rocky reefs, and rubble and reinforced concrete blocks (dolosse) around the seaward slopes of the airport runway. The lagoon is mostly soft muddy bottom with scattered rocks and dead corals. It is partly enclosed by the airport runway with the remaining shoreline composed of rocky reef or soft sediments, and red mangroves (Rhizophora mangle).

Acoustic array
The acoustic monitoring system consisted of 45 omnidirectional receivers (VR2W, 69 kHz, Innovasea Systems Inc. (previously Vemco), Halifax, Nova Scotia, Canada) that were moored, and spaced equally across Brewers Bay, including eastern Perseverance Bay, and along the southern side of the airport runway (Fig. 1). Range testing of receivers [24] across the study site was conducted over four days in June 2015, by placing receivers in depths ranging from 5 to 19 m over different substrate types including shallow and deep coral/rock and seagrass/sand [25]. Probabilities of transmission were tested using three A69-1601 Inno-vaSea transmitters V9-2H (151 dB), V13-1H (153 dB) and V16-4H (158 dB) that transmitted every 60 s. Transmitters were attached to mooring lines, connected to cinder blocks, and suspended 1 m above the bottom. A detection probability of 70% for V13-1H transmitters was selected providing high coverage throughout the study area with estimated detection ranges of 101 m in seagrass/sand and 120 m in coral/rock substrates (Fig. 1). Seawater temperature and dissolved oxygen (DO) were collected at several stations in Brewers Bay using Hobo temperature loggers (Onset Computer Corporation, Bourne, MA, USA) and miniDot DO loggers (Precision Measurement Engineering Inc, Vista, CA, USA) that were attached to acoustic receiver moorings. Temperature loggers were deployed in August 2015, DO loggers were deployed in February 2016, and both recorded data at 15-min intervals (Fig. 1).

Fish capture
All capture and tagging methodology in Brewers Bay was approved by the University of the Virgin Islands Institutional Animal Care and Use Committee (IRB #747807-1). Juvenile Atlantic tarpon were caught using hook and line from a boat or dock between September 2015 and November 2016. As each fish was reeled in, it was guided alongside the boat or dock and into a floating cradle constructed of PVC pipe, plastic mesh, and foam noodles for buoyancy. Once in the cradle, the fish was held under water, turned upside-down to induce tonic-immobility, and the hook was removed from the mouth. Each fish (n = 14) was measured for fork length (FL) and total length (TL) to the nearest millimeter (mm). Acoustic transmitters (either V13 [13 mm × 36 mm; n = 8] or V13P [13 mm × 46 mm; n = 6; pressure tags that provide depth data], 69 kHz, Innovasea Inc, Halifax, NS, Canada) were surgically implanted into the body cavity on the ventral side of the fish [26]. The incision was closed with surgical staples and treated with antibacterial ointment (note: antibacterial ointment is no longer used on incision and sutures). Fish remained immersed in open seawater the entire time so no general or local anesthetic was administered, which allowed for the release of fish shortly after tagging and data collection were completed. Fish were turned back over, the head was faced into the current to increase ventilation, and after a few minutes of recovery, fish were released at the capture location (Fig. 1).

Data processing
Detections were downloaded from receivers every 3 months and analyzed using R Version 3.4.3 [27]. For each 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 each individual tarpon by receiver were plotted through time to investigate the presence of dropped tags, dead individuals, and short-term residency. Of the 14 juvenile tarpon that were tagged, four (n = 4) individuals had at least 1 month of tracking data to conduct spatial home range analysis. Three of these tarpon were detected for 344-472 days and also had pressure transmitters, thus were used to analyze monthly and seasonal trends in rates of movement, activity space, and vertical distribution (Table 1). Of the remaining ten tarpon that were excluded from analysis, eight (n = 8) were within the array two days or less and had insufficient detections for analyses, and two (n = 2) had either died or shed their tags (Table 1).
Temporal data were examined for seasonal and diel patterns. Seasons were defined as spring (March, April, May), summer (June, July, August), fall (September, October, November) and winter (December, January, February). Crepuscular periods were calculated using astronomical twilight based on daily sunrise/sunset time charts for Charlotte Amalie, St. Thomas, U. S. Virgin Islands [28]. Specifically, dawn was defined as − 1 h before astronomical morning and + 1 h after sunrise to account for seasonal changes in day length. Likewise, dusk was defined as − 1 h before astronomical twilight to + 1 h after sunset. Day and night periods were the remaining hours between bracketed dawn and dusk, respectively.

Data analysis and statistics
Residency index was calculated for the four fish used in analyses by dividing total days each fish was detected within the Brewers Bay array by number of days between the first and last detection. Residency Index was defined as the percentage of days spent within Brewers Bay array for the duration of time that each fish was tracked.
Center of activity (COA) for juvenile tarpon (n = 4) was calculated every 30 min using mean position (latitude and longitude) of all detections during that time step [29]. Distance between COA relocation points and difference in time between each relocation point were calculated for each fish using 'adehabitatLT' package of R environment [30]. COA values were used to calculate rate of movement (ROM) and activity space for individual fish, and included minimum convex polygons (100% MCP) and kernel utilization distributions (50% and 95% KUD).
Activity space, which incorporates MCP, 50% KUD and 95% KUD, was calculated using the 'move' and 'adehabitat' package in R environment [30,31]. MCPs provided information on the extent of an individual's range or area used and included all outlying points that might be the result of exploratory movement or periodic migration not part of their typical activity. KUDs highlight the density of positions of an individual within the activity space based on COAs (i.e., 50% KUD = high density, 95% KUD = low density), as well as estimated error around these positions [32,33]. When necessary, a 'land' barrier polygon was used to clip out the area of MCP and KUD polygons that fell on land ('rgeos' package, [34]). The calculated MCP and KUD (50% and 95%) activity spaces were plotted in ArcGIS 10.6 for annual, monthly, and diel periods. To calculate the degree of overlap in 50% and 95% KUD among individuals over diel and monthly time periods, a home range (HR) percent overlap analyses was applied using the 'kerneloverlaphr' function of the 'ade-habitatHR' package [30,35,36]. The HR percent overlap analyses calculates the proportion of animal a's home range that is overlapped by animal b's home range [30,35,36]. The data output matrix provides indices of overlap for all pairs of animals [35,36]. Using the matrix output, average and ranges in fish overlap values were calculated. Repeated measures analyses of variance (RM-ANOVA) was used to test for differences in KUD across monthly and diel periods. All monthly analyses used data from three (n = 3) tarpon that had average KUD activity space representing each month (Table 1). Individual tarpon were treated as random variables, and either monthly or diel periods were treated for autocorrelation effects ('corAR1') using the 'lme' function of the 'nlme' package for R [37,38]. To assess relationship between monthly ROM and 50% KUD size, a linear regression was applied.
Rate of movement (ROM, m/s) was calculated by dividing the distance between consecutive COA position values by the time difference between these consecutive points. Kruskal-Wallis and Tukey post hoc tests were used to test for differences in ROM between diel periods and a two-way ANOVA was used to test for differences in diel ROM across seasons. ROM provides a useful metric for fish activity during diel periods and can also be used as a proxy for feeding behavior [47].
Vertical distribution was calculated for tarpon tagged with depth-enabled transmitters (n = 3, Table 1). Depth measurements were binned into hourly and monthly periods and boxplots were applied to elucidate their vertical movement patterns. ANOVA and Tukey post hoc tests were used to test for differences in vertical movement across diel and monthly periods.
Environmental conditions and their relationship to tarpon movement and habitat use were assessed for seawater temperature and DO. Daily average number of detections, average temperature and average DO within the lagoon and waters along the airport runway were analyzed by applying a linear regression for the study period (September 2015-February 2018).

Results
Fourteen (n = 14) juvenile tarpon were captured and acoustically tagged in Brewers Bay (average FL 83.7 cm, range 61-95 cm; Table 1). Only four (n = 4) juvenile tarpon provided a sufficient number of detections over a sufficient duration (32-472 days), and a residency index of 78-100%, to be included in our spatial analysis (Table 1). Eight (n = 8) fish were detected for less than a week and had fewer than 1000 detections and upon assessment, it was determined that the two remaining fish detected within the bay had died or shed their tags within one day following release.

Activity space
The activity space of juvenile tarpon varied among individuals and through time. The average MCP for juvenile tarpon (n = 4) was 0.97 km 2 (range 0.77-1.17 km 2 ), while the average 95% and 50% KUD was 0.76 km 2 (range 0.49-0.99 km 2 ) and 0.13 km 2 (range 0.08-0.20 km 2 ), respectively (Table 2; Fig. 2). Comparison of mean day, Table 2 Calculated home range size (km 2 ) 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 a In this case 100% MCP is smaller than 95% KUD based on how they are calculated (see "Materials and methods")  , 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. night and crepuscular activity spaces among juvenile tarpon for both 50% and 95% KUDs were not significantly different across diel and crepuscular periods (50% KUD: p = 0.07; 95% KUD: p = 0.44) and across months (50% KUD: p = 0.78; 95% KUD: p = 0.29).

Fish ID
Analysis of daytime activity space overlap averaged 12% for 50% KUD and 42% for 95% KUD during the year (Table 3), with each tarpon showing distinct 50% KUD core areas centered around northwest corner of runway (ID#36032), around Black Point and deeper part of Brewers Bay (ID#2966), in and around the lagoon and Range Cay extending to shallow and deep parts of Brewers Bay (ID#10979), and around the tip of runway (ID#10980) (Fig. 2, day). In April, however, overlap for 50% and 95% KUD during daytime showed an increase to 20% and 63%, respectively (Table 3). Excluding the month of April, daytime 50% and 95% KUD overlap values declined from 12 to 2% and 42% to 23%, respectively (Table 3). At nighttime, 50% KUD areas were centered in shallow Brewers Bay, around the airport runway and particularly inside the shallow lagoon, where juvenile tarpon went at night (Fig. 2, night). Consistent use of these areas at night tended to increase nighttime 50% and 95% KUD overlap relative to daytime, except for April, when space overlap decreased at night ( Table 3).

Vertical movement
Vertical movement of juvenile tarpon with pressure transmitters (n = 3) varied among time of the day (ANOVA: F 1,3 = 36,526, P < 0.0001) (Fig. 4). Tarpon used more of the water column during the day ranging between 2 to 13 m average depth and 16 to 27 m maximum depth (Fig. 4). At night, tarpon stayed in shallower waters ranging from 0 to 5 m average depth and 8 to 14 m maximum depth ( Fig. 4; Additional file 1: Table S1). Nighttime vertical movements were partly constrained when tarpon were in lagoon (maximum depth 4 m, Fig. 2). During dawn and dusk, average depth of tarpon ranged between 0 to 8 m ( Fig. 4; Additional file 1: Table S1). Vertical distribution across months showed no consistent patterns among the three tarpon with depth transmitters.

Movement and environmental variability
Water temperature in Brewers Bay ranged from 25-28 °C in winter to 29-32 °C in late summer and early fall. Inside the lagoon water temperature showed greater fluctuations on a daily basis and had a greater range (mean = 28.3 °C ± 1.27 SD, range = 24.8-32.0 °C) than in the bay (mean = 28.1 °C ± 1.15 SD, range = 25.6-30.6 °C) (Fig. 5). Water temperature had a strong effect on tarpon movement and habitat use. We found a significant negative relationship between number of tarpon detections and temperature in the lagoon at night (adjusted R 2 = 0.0.32; P < 0.001), but no relationship between frequency of detections in the lagoon or around the runway at other times of day (Fig. 6). Juvenile tarpon were present in the lagoon at night when temperature ranged between 26 and 28 °C; however, once temperature reached 29 °C frequency of tarpon detections decreased rapidly and stopped at about 30.5 °C (Fig. 6), indicating tarpon left the lagoon. Water temperatures in the lagoon reached or exceeded 30.5 °C on 59 day of the study period compared to only 4 days at the airport runway. Likewise, water temperatures 26 °C colder were recorded on 61 day in the lagoon but only on 16 day along runway. At times of high lagoon temperatures, juvenile tarpon left the lagoon and had higher frequency of detections at night along the tip and south side of the airport runway (i.e., stations 248, 249, 285, 251, 282; Fig. 1), where nighttime maximum water temperatures were cooler (Figs. 5, 6a). When water temperatures in lagoon cooled to below 30.5 °C, juvenile tarpon returned to resting in lagoon at night (Fig. 5).
Similar to water temperature, dissolved oxygen concentrations in the lagoon varied widely from 0.9 to 7.1 mg/L (mean = 4.7 ± 1.89 SD), but were more stable along the airport runway (mean = 6.1 ± 1.9 SD, range 5.3-6.6 mg/L) (Fig. 5). Based on detection frequencies, there  , February). b Relationship between average ROM and core activity space 50% KUD for four juvenile tarpon during each month was no significant relationship in number of detections of tarpon at different levels of dissolved oxygen within the lagoon or the runway (Fig. 6b), indicating that tarpon seemed to tolerate the low oxygen levels in the lagoon, especially at night

Discussion
To our knowledge, this study provided some of the first data on small-scale three-dimensional movement patterns of juvenile Atlantic tarpon (n = 4) by way of passive acoustic telemetry. The data can serve as a baseline for juvenile tarpon movement ecology that can further be examined and use for comparison to adult movements or other regions [6,22]. Although most juvenile tarpon (n = 8) left the bay shortly after tagging and their fate remained unknown, and two fish likely died or shed their tags, the remaining four fish provided useful data on the movement ecology of juvenile tarpon. Juvenile tarpon were resident within the bay 78% to 99% of time, but some transient behavior was observed for two of the larger individuals (i.e., both were 95 cm FL). One tarpon (ID #10979) left the bay for nearly 2 months (October and November) before returning to its home range for another 7 months. The second tarpon (ID#3032) remained within Brewers Bay for 1 month before departing mid-October, but it was then detected at an acoustic array 12 km offshore in January. Interestingly, both tarpon departed in October when water temperature was high. Seasonal movements, such as these, by Atlantic tarpon and other coastal species have been attributed to food availability, reproductive maturity (spawning aggregations) and changes in environmental conditions (i.e., temperature, dissolved oxygen) [6,13,15,16,[39][40][41].
We found that juvenile tarpon had distinct daytime 50% KUDs, and core areas (0.07-0.20 km 2 ) within Brewers Bay that overlapped very little with the other individuals for most of the year (< 2%). At night, tarpon tended to move into or near a small, shallow lagoon in Brewers Bay, which resulted in an increase in overlap of 50% KUDs during most months. The spatial patterns displayed by juvenile tarpon suggest habitat partitioning during daytime and sheltering and protection from predation in a common area at night [6,13,17,18,42]. During April, however, daytime overlap in 50% KUD area showed a tenfold increase, as they shifted their activity space to similar areas within Brewers Bay. These changes in behavior and activity space coincided with the arrival of schools of bait fish as well as nesting seabirds that feed on these schools in the spring [43,44]. When seabirds were present, we observed groups of tarpon foraging on bait fish near the surface during the spring months primarily in the middle of Brewers Bay and near Black Point reef (Duffing Romero, M. and Nemeth, R.S., pers. observations). This feeding strategy is not uncommon for tarpon and other pelagic predators, which can increase their foraging success in the presence of seabirds feeding on bait fish at the water surface [15,43,45]. The areas of Brewers Bay where this feeding behavior was observed corresponded to April daytime activity space of tagged tarpon. Adult tarpon tend to feed at sunset and continue feeding into the night if there is enough food and available light for foraging [15,46]. As with other species [47], ROM was assessed as a proxy for feeding. Similar to adult tarpon, juveniles had the highest rates of movement during dawn and dusk, which suggests high feeding rates during crepuscular periods. However, this behavior may also indicate rapid movements along migration pathways between nighttime and daytime activity spaces [18,[48][49][50][51][52][53][54]. ROM was significantly slower at night than other time periods, which suggests that juvenile tarpon were not feeding at this time. Further research with improved experimental design will help to distinguish differences between adult and juvenile behavioral states such as resting, foraging or traveling [55].
Juvenile tarpon generally stayed less than 10 m depth, but occasionally went to 25 m or deeper, which is also typical for adult tarpon [6,13]. Many coastal and pelagic fish, such as barracuda (Sphyraena barracuda), white marlin (Kajikia albida), dolphinfish (Coryphaena. hippurus) and many species of tuna (Thunnus spp) show similar vertical movement patterns, where they spend the majority of time at shallow depths or close to the surface and then make diel/seasonal deep water movements [56][57][58]. Adult tarpon show a variety of vertical distributions that fall into four typical patterns: (1) clear diel pattern shallow in day and deep at night; (2) deep in day and shallow at night; (3) deep and shallow at irregular intervals throughout diel period, and (4) random vertical movements throughout diel period [6]. Juvenile tarpon in Brewers Bay showed a consistent diel vertical movement pattern that matched pattern (2) where fish stayed shallow at night and deeper during the day. At smaller sizes juvenile tarpon may select shallow, sheltered lagoon-type habitats, if available, as a strategy against predation [14,15]. In this study, all four tarpon used the Brewers Bay lagoon consistently throughout most of the year. Environmental conditions influenced tarpon behavior in Brewers Bay. Tarpon prefer water temperatures from 24 to 26 °C in spring and fall and 28-30 °C in summer [6,13,23]. We found that juvenile tarpon avoided water temperatures greater than 30 °C. For instance, tarpon detection frequencies within the lagoon decreased at temperatures above 29 °C and they did not enter nor rest in the lagoon at night when water temperature was higher than 30.5 °C, but instead moved to deeper water on the south side of airport runway (Fig. 5). At this threshold temperature, tarpon faced a trade-off of remaining in higher temperatures within the protected lagoon or leaving the lagoon for cooler, less protected waters around the airport runway at night. Previous studies on barracuda and bonefish (Albula vulpes) have shown that both species move to deeper waters away from their home range to avoid seasonal weather patterns and associated temperature fluctuations [15,39,59]. Adult tarpon in Florida migrated farther northward on a daily basis as sea surface temperatures increased and seemed to track the 26 °C isotherm from the Florida Keys to the southern coast of Virginia from May to July, respectively [6]. Despite the effect of high water temperatures on tarpon behavior, tarpon tolerated low dissolved oxygen concentrations in the lagoon, which is attributed to being facultative air-breathers [13,60].

Conclusion
To our knowledge, this acoustic telemetry study provided some of the first information on juvenile tarpon movement ecology including home range size, rates of movement, vertical distribution, and habitat partitioning. Although limited to only four fish, our results showed 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 over multiple years showed the effects of changing environmental conditions on juvenile tarpon movement and habitat use. These baseline observations highlight the need for more extensive studies of juvenile tarpon across a broader range of their distribution. In addition to a larger sample size, we suggest including a wider range of tarpon size classes, from small juveniles to large reproductive adults, in future studies. Since tarpon are highly mobile but also show resident behavior [6,7,13,40], it is difficult to assess their larger-scale movement patterns using an acoustic array limited to one bay. A better approach, to facilitate tracking tarpon movements over a broader geographic range, would be to tag tarpon with both acoustic and satellite tags and place additional receivers along the coastlines or use a regional network within and among neighboring islands [9,40,61,62].
Abbreviations COA: Center of activity; MCP: Minimum convex polygon; KUD: Kernel utilization distribution; ROM: Rate of movement; HR: Home range.