Environ Biol Fish DOI 10.1007/s10641-017-0654-6

Summer and fall movement of cownose ray, Rhinoptera bonasus, along the east coast of United States observed with pop-up satellite tags Kristen L. Omori

&

Robert A. Fisher

Received: 28 September 2016 / Accepted: 3 August 2017 # Springer Science+Business Media B.V. 2017

Abstract Cownose ray, Rhinoptera bonasus, is a common elasmobranch species along the southeast United States coast that recently has received negative attention. These rays can consume considerable amounts of commercial shellfish raising concerns regarding their control and need for effective management. However, limited information is known regarding their population abundance and migration patterns. We addressed the latter by reviewing 25 tagged cownose rays in Chesapeake Bay with pop-up satellite archival tags (PSATs) to study their movement patterns during summer and fall and identify wintering grounds. Eleven tags provided useful data on temperature, depth, light level and/or end locations. The migration tracks were deciphered through geolocation based on light levels, sea surface temperatures and depth constraints. PSAT end locations indicated southern wintering grounds in the coastal waters of central Florida. Female rays migrated out of Chesapeake Bay at the end of September to early October and continued their southerly migration to Florida. Male rays exited the bay in July and migrated northward based on their estimated movement tracks. The male rays appeared to have a second summer feeding ground off the coast of southern New England. In the fall, males migrated south from New England to the same wintering grounds as the females. No diel differences in habitat use were detected; however, males tended to occupy a wider depth and K. L. Omori (*) : R. A. Fisher Virginia Institute of Marine Science, College of William & Mary, P.O. Box 1346, Gloucester Point, VA 23062, USA e-mail: [email protected]

temperature range compared to females. Information on the movement patterns and habitat use for cownose rays will assist in determining more effective recreational and commercial management plans. Keywords Batoid . Electronic tags . Movement patterns . Migration routes . Habitat use

Introduction Cownose rays (Rhinotpera bonasus) are a myliobatiod species that are distributed from along the coastal waters of eastern United States to Brazil (Bigelow and Schroeder 1953) and Gulf of Mexico (McEachran and Fechhelm 1998). This highly migratory species is a seasonal inhabitant productive estuaries along the United States east coast. A portion of the overall migrating ray populations migrates into Chesapeake Bay to use the ecosystem for mating and nursery grounds during the late spring and summer (Fisher 2010). Although cownose rays are epipelagic and are commonly seen at the surface individually or in large aggregations (<5,000,000 rays), the rays are benthic feeders (e.g., Rogers et al. 1990; Blaylock 1993). Cownose rays are durophagous feeders (i.e., eating hard-shelled prey), consuming a wide range of benthic organisms including molluscs, crustaceans, benthic polychaetes, but primarily bivalves (Smith and Merriner 1985; Collins et al. 2007; Fisher 2010). Cownose rays prefer softer-shelled bivalves (Fisher et al. 2011), such as bay scallops (Argopecten irradians) and soft-shelled clams (Mya

Environ Biol Fish

arenaria). Previous studies found that top prey items for this species in Chesapeake Bay were soft-shell clams and Baltic macomas (Macoma balthica), whereas hardshelled bivalves were not as common in their diets (Merriner and Smith 1979; Smith and Merriner 1985; Fisher 2010). However, the rays appear to be opportunistic feeders and tend to target areas with higher prey density (Smith and Merriner 1985; Collins et al. 2007; Fisher et al. 2011). The wild shellfish population in Chesapeake Bay has been in a precipitous decline since the Europeans arrived due to intense harvesting, declining water quality and disease (e.g., Paolisso et al. 2006). As a result there has been an increase in aquaculture and habitat restoration efforts for eastern oysters (Crassostrea virginica; Luckenbach et al. 2005; Murray and Hudson 2015) and hard-shell clams (Mercenaria mercenaria; Murray and Hudson 2015). For the past four decades, there have been increasing concerns regarding predation by cownose rays on the declining commercial shellfish populations in Chesapeake Bay (Merriner and Smith 1979; Smith and Merriner 1985; Fisher 2009). Peterson et al. (2001) blamed the ray for the decline of bay scallop populations in North Carolina, stating that schools of rays can exploit and effectively reduce dense areas of scallops. Claims have been made that the cownose ray population in Chesapeake Bay has increased dramatically and consequently is placing significant pressure on shellfish aquaculture and habitat restoration in the bay (Merriner and Smith 1979). However, these claims have been recently debunked by Grubbs et al. (2016), who demonstrated the lack of correlation between the increase in ray abundance and major shellfish declines. Only one study has attempted to estimate the cownose ray abundance in Chesapeake Bay. The aerial surveys from Blaylock (1993) indicated a wide variation in the average abundance of cownose rays throughout the summer, with the counts ranging from no rays to a high monthly average estimated at 9.3 million in September from 1986 to 1989. This high variation likely reflects measurement error due to the patchy distribution of the rays and variability in sight ability. Unfortunately, because there is a lack of historical and present data to compare to Blaylock’s abundance estimates, the estimated stock size of the cownose ray population and trends in its abundance in Chesapeake Bay are unknown. The notoriety of the species has caused pressure to manage their destruction of commercial shellfish. In

2007, despite the lack of abundance surveys and to ameliorate potential pressure of predation on shellfish, a fishery for cownose rays was launched and subsidized by the Virginia Marine Resources Commission (Fisher 2010). Because this fishery was unregulated and unmanaged and because rays have life history characteristics that make them susceptible to fishing pressures, these factors may lead to a Bboom and bust^ situation as has been observed in other fisheries (e.g., orange roughy, Hoplostethus atlanticus, fishery; Clark 2001). In recent years, recreational bow-hunting for cownose rays has grown in popularity, with some tournaments simply interested in ray removal with the belief of benefiting shellfish resources. This recreational fishery, along with increased pressure for a targeted or bycatch commercial fishery has prompted NOAA Chesapeake Bay Program and state managers to compile cownose ray life history, population dynamics, fishing effort, and ecosystem interaction information to identify a mechanism to determine stock status for management framework (Franke et al. 2016). The life history characteristics of the cownose ray follow the BK-selected^ traits (e.g., late maturity, low fecundity, large maximum size and high maximum age) similar to other elasmobranchs (Hoenig and Gruber 1990; Musick 1999), which make this species vulnerable to overexploitation. Studies have shown that cownose rays do not become fully mature until reaching ~70% of their maximum size, which equates to around seven to eight years for females (85–88 cm disc width) and six to seven years for males (>85 cm disc width) (Smith and Merriner 1987; Fisher et al. 2013). The oldest individual female observed was estimated to be age 21 years and the oldest estimated age for males was 18 years (Fisher et al. 2013). Females generally have one offspring per year, pupping in late June- early July after an 11–12 month gestation period (Smith and Merriner 1986; Fisher et al. 2013). However, there have been a few documented cases of twins (Fisher et al. 2014). Immediately following parturition, mating occurs. Cownose rays are susceptible to fishing pressure throughout their summer residency (May–October) in Chesapeake Bay, during which mature females are carrying either late-term (May–June) or early- term (July–October) embryos. As such, with the removal of each adult female, a cohort is also removed. These life history characteristics generally indicate a slow population growth potential.

Environ Biol Fish

Short segments of the annual migration patterns of cownose rays in Chesapeake Bay have been identified in several studies. Both males and gravid females are observed off the coast of North Carolina in April and enter Chesapeake Bay in the beginning of May (Smith and Merriner 1987; Blaylock 1993; Fisher 2010). This species is abundant throughout the summer in the bay with high variation in school size. The rays exit the Bay in October (Merriner and Smith 1979; Blaylock 1993; Fisher 2010) for the start of their fall migration to their wintering grounds. This is also consistent with their seasonal patterns in North Carolina waters (Goodman et al. 2011). However, only the females and pups occupy the shallow estuarine waters of Chesapeake Bay from late July through October (Fisher 2010). Grusha (2005) suggested that the wintering nursery habitat for female cownose rays is off the east coast of Florida based on five tags deployed in 2003. Four of the tags resulted in detailed data recovery, but none produced reasonable movement tracks. Only possible wintering grounds for female rays were inferred from the tag release location. The male residency time inside Chesapeake Bay, subsequent movements in the summer, and the fall migration track are poorly known. Habitat utilization and migration routes for both sexes of cownose rays are important features of their life cycles to understand in order to provide appropriate management strategies in the Chesapeake Bay. The goals of this study are: 1) identify the wintering grounds, 2) determine summer and fall timing and migration route, and 3) examine temperature and depth preferences for female and male cownose rays. We hypothesized that the male and female rays comingle in their winter habitat in the coastal waters of Florida based on predicted winter habitat for the females from Grusha (2005). No studies on the Atlantic coast specifically targeted male movement or habitat use. We expected there to be small differences in preferred depths and temperatures due to the males being absent in the shallow waters of Chesapeake Bay during the summer. We tagged the rays with pop-up satellite archival tags (PSATs), which are suitable electronic tags for this ray species based on minimal metabolic cost imposed by the drag of the tag on large rays (>14.8 kg; Grusha and Patterson 2005). We analyzed the temperature, depth and light-level profiles from the tags for geolocation information to address these goals.

Methods Tagging and deployment A total of 25 mature cownose rays were captured, tagged and released in Chesapeake Bay during the summers and early falls from 2009 to 2011 and 2013 (Table 1). The rays were caught by local fishermen using haul seines in the Back River Inlet in the Poquoson River, Virginia, and transported to a large holding tank (4.3 m × 6.4 m x depth 0.71 m) at the Virginia Institute of Marine Science (VIMS; 37.247°N, 76.505°W) (Fig. 1). The animals were acclimated for 72 h in the tank with flow-through seawater before being subjected to handling and tagging under established Institutional Animal Care and Use Committee (IACUC) protocols (IACUC-2012-07-09-8040rafish). Female rays were targeted in mid-September to early-October 2009–2011 (n = 14), and in 2013, male cownose rays were targeted mid-June through early July (n = 11). Only healthy rays (i.e., normal swimming behavior and no discoloration or wounds on their bodies) were selected to be tagged with PSATs (Mk10-PAT in 2009 and 2010, MiniPAT in 2011 and 2013, Wildlife Computers, Redmond, WA). The tagged females ranged from 95.0 cm to 103.5 cm in disc width (DW) and males ranged from 89.0 to 94.5 cm DW (Table 1). Each ray selected for tagging was first anesthetized with tricaine methanesulfonate (MS-222), and then transferred to the tagging station. The PSAT was attached to each animal by suturing a loop of 200 lb. nylon fishing line through and around the base of the muscular part of the tail just forward of the small second dorsal fin (as described in Le Port et al. 2008). This method provided a central placement of the tag and minimized drag. This method has been performed successfully on a variety of batiod species (e.g., short-tailed stingray, Le Port et al. 2008). After the tagging procedure, the ray was placed in a recovery pool and then returned to the large holding tank. Tagged rays were held in the holding tank for 24 h to ensure the tagging process was successful and the health of the ray appeared normal before individuals were released into the York River off the VIMS beach (Fig. 1). Most of the satellite tags were programmed to be released from the ray after the end of the fall migration in mid-December. Different days at liberty reflect when the rays were tagged relative to a date after which

Environ Biol Fish Table 1 Summary of cownose rays (Rhinoptera bonasus) in Chesapeake Bay that were tagged with pop-up satellite tags from 2009 to 2013. All rays were released at 37.247°N latitude,

76.505°W longitude. Tag retention categories: ‘E’ = early release of tag from ray, ‘M’ = missing/ no reporting after deployment, ‘OT’ = on time release, ‘Preyed’ = tag was consumed

Ray # Sex (DW in cm) Release date Report date Report latitude (°N) Report longitude (W) Days at Tag At Cape Hatteras liberty retention 1

F (100.0)

10/2/2009

10/13/2009 35.98

−75.501

11

E

10/13/2009

2

F (100.0)

10/3/2009

-

-

-

M

-

3

F (97.5)

10/3/2009

10/16/2009 36.39

−75.702

9

E

10/23/2009

4

F (102.0)

10/2/2009

1/9/2010

40.40

−58.850

100

OT

11/5/2009

5

F (96.5)

10/2/2009

-

-

-

-

M

-

6

F (95.0)

10/3/2009

-

-

-

-

M

-

7

F (91.5)

10/2/2009

10/12/2009 -

-

-

Preyed

-

8

F (101.5)

9/29/2010

11/1/2010

31.88

−80.244

33

E

10/17/2010

9

F (103.5)

9/29/2010

10/10/2010 34.88

−76.062

12

E

10/7/2010

10

F (97.0)

9/15/2011

12/13/2011 28.08

−80.561

89

OT

10/3/2010

11

F (96.0)

9/15/2011

12/13/2011 28.13

−80.579

89

OT

NEI

12

F (100.0)

9/16/2011

12/15/2011 28.83

−80.761

90

OT

10/8/2011

13

F (98.0)

9/15/2011

9/19/2011

-

-

5

E

-

14

F (95.0)

9/15/2011

9/19/2011

-

-

5

E

-

15

M (92.5)

6/13/2013

6/25/2013

-

-

13

E

-

16

M (90.5)

6/14/2013

7/15/2013

37.50

−74.578

32

E

-

17

M (90.0)

6/14/2013

6/18/2013

34.50*

−77.157*

5

E

-

18

M (93.0)

7/6/2013

12/2/2013

27.03**

−80.095**

147

OT

10/29/2013

19

M (93.5)

6/13/2013

6/18/2013

-

-

6

E

-

20

M (91.0)

6/14/2013

7/9/2013

38.29*

−76.107*

26

E

-

21

M (89.0)

6/13/2013

10/11/2013 36.45

−75.723

119

OT

10/11/2013

22

M (94.5)

7/5/2013

7/11/2013

32.50

−78.515

7

E

-

23

M (90.5)

6/14/2013

-

-

-

-

M

-

24

M (93.5)

7/6/2013

7/25/2013

37.00*

−76.118*

20

E

-

25

M (93.0)

7/6/2013

11/30/2013 28.15

−80.584

145

OT

NEI

-

NEI, Not Enough Information * Tag end location in Chesapeake Bay ** Estimated latitude and longitude based on tag being found at Blowing Rock Conservatory, Jupiter, FL, USA

wintering grounds were reached. For example, the tags deployed on the female rays tagged in September or October were programmed to be released after 90 d in 2010 and 2011 and 100 d in 2009, and the tags on males tagged in June or July were set to detach between 100 to 150 d. The satellite tags were programmed to be released prematurely if the animal stayed at a constant depth (constant pressure) ± 2.5 m for 24 h for 2009– 2010 tags and 72 h for 2011 and 2013 tags or went below 4000 m depth for 2009–2011 tags and 1700 m depth for 2013 tags. The sensors were set to record every 3 or 5 s. The compressed information transmitted to the satellites as a 24 h summary period with 12

temperature and depth bins, along with one set of dawn-dusk light curves when available. If the tag was recovered, the complete archive was accessible. Tag analysis for movement patterns We used a variety of methods and programs to solve for the geolocations and the best estimated migration track, which is referred to as the most-probable-track. Geolocations are calculated based on light levels estimated from dawn and dusk of the local area, which can be used to delimit latitude and longitude. The estimated geolocations tend to have many sources of error, with

Environ Biol Fish

Fig. 1 Start (square) and end locations of pop-up satellite archival tags (PSATs) that were deployed on cownose rays for more than 10 days and migrated out of Chesapeake Bay (triangles) and end locations of tags from Grusha (2005) study (circles). The end location for Ray 4 (F, 1/9/2010) is outside of the map boundaries, but is shown in Fig. 2

estimated longitudes having better accuracy than latitudes. Longitude is determined by the local noon and is not influenced by the latitude and time-of-year, whereas it can be difficult to estimate latitude during equinoxes and at lower latitudes (Hill 1994; Musyl et al. 2001). The tag pop-up location (end location) is generally known with much more precision (within 1.5 km) from the passing Argos satellites established by the first transmission with an Argos location class of 3, 2 or 1 (Argos 2015). We downloaded and decoded the archived information on light-level, temperature and depth as well as the end location in the manufacturer’s software program (WC- DAP 3.0, Wildlife Computers, Redmond, WA). We calculated the geolocations and migration tracks for the rays whose tags were deployed for over 20 d and migrated out of Chesapeake Bay (four females and three males; Table 1). The time interval ensured that we examined large scale movement patterns. Ray 16 was excluded from the analysis because the end location indicated the ray had recently exited the Bay and had not begun the summer migration. We used the state-

space Kalman filter (Harvey 1990) to determine the most-probable-track given in estimated geolocation coordinate pairs using the random walk model described by Sibert et al. (2003), in the KFTRACK package. This is an add-on package for the statistical environment R (R Core Team 2012). We also used an improved version of the model, unscented Kalman filter with sea surface temperatures (UKFSST), described by Lam et al. (2008). Additionally, we ran the light levels through Wildlife Computers’ global estimation version 3 program (WC-GPE3) to analyze the geolocations, which uses a gridded hidden Markov model using the forwardbackward algorithm (Heather Baer, pers. comm.; also see Basson et al. 2016). A secondary bathymetric correction based on maximum depths was used on all converged tracks from the different models to verify or reject the estimated geolocations (Hoolihan 2005; Teo et al. 2007; Galuardi et al. 2010). In addition to using state-space modeling to delineate the most-probable-track for cownose rays in Chesapeake Bay, we examined only longitudes because estimated longitudes are more accurate than estimated latitudes (Hill 1994; Musyl et al. 2001). We compared the estimated longitudes throughout the tag deployment from two programs (UKFSST and WC-GPE3) to the longitudes along the east coast of the United States (coastline longitudes). Thus, if the rays were assumed to follow the east coast of the United States as they traveled to their wintering grounds, the longitudes of the coastline should match the longitudinal tracks from the programs. This analysis was conducted for the tags that were released on schedule and detailed data from the tag was transmitted. We calculated migration rates (km/day) from Cape Hatteras, North Carolina, USA to their end locations in the southern feeding grounds. The migration rates were determined by two methods. The first method used the sum of the distances traveled in kilometers between each estimated geolocation from WC-GPE3 starting from the first estimated location south of Cape Hatteras divided by the total number of days traveled to their end location. Because the number of geolocation points estimated was different for each ray, we calculated a second migration rate based on an average pathway. The distance measured along the average pathway ended nearest to the end location for each ray. This average pathway does not account for stray individual movements. These two migration rates gave a possible rate and a minimum rate, respectively.

Environ Biol Fish

Tag analysis for environmental preferences and vertical movements Environmental preferences and daily movement patterns were inferred from the temperature and depth measurements for rays at liberty for more than 20 days and migrated out of Chesapeake Bay to examine differences in the habitat use. Three females and three males were used for the analysis. To assess any possible diel differences in habitat utilization and behavior through the depth and temperature records, two diel periods, day and night, were considered. The day captured a six hour period from 08:00 to 16:00 h and the six hour period from 21:00 to 05:00 was designated as night. To assess potential differences in mean depth and temperature between the two diel periods, night and day, and the sex of the ray, linear mixed effects models with repeated measures were used with a total of 455 observations. The repeated measures analysis was used to account for the correlation of the replicates in the dataset due to the multiple observations for each individual ray. The base linear mixed effects model is as follows: Y ijkl ¼ μ þ δi þ ω j þ ρk þ τ l þ εijkl Here, Yijkl is the mean depth or mean temperature in time period i (i = day or night), for sex j (j = male or female), for individual ray k, and specific Julian date l. Yijkl is modeled as a function of the overall mean, μ, time period, δi, sex of the ray, ωj, effect of the individual ray, ρk, Julian date, τl, and random error, εijkl. All factors except the effect of the individual ray and error term were treated as fixed effects. Each factor was added to the model to determine the amount of influence it has on the mean temperature or depth. The depth data were log transformed (loge) to meet the assumptions of the model. The error terms for the mean depth (after the transformation) and mean temperature were normally distributed (εijkl ~ N(0,σε2)). All combinations for possible interactions were examined and tested. Because the time period (night and day) both occur in each day, the time period was nested in the Julian date. The repeated measures were addressed by specifying a covariance structure that allowed for correlation among the error terms. Akaike’s information criterion (AIC, Akaike 1973) was used to select the most appropriate covariance structure (autoregressive 1, compound symmetry, unstructured,

Toeplitz and variance components). The statistical analysis was performed in SAS (version 9.3, SAS Institute, Cary, NC).

Results Deployment duration and data retrieval From the 25 PSATs deployed, seven tags successfully detached on the scheduled date (four females and three males), ranging from 89 to 147 d at liberty (Table 1). One of these successful tags did not transmit any messages after the scheduled release, but was found and returned a year later by a beachcomber. Four of the tags were never heard from after the ray was tagged and released. One tag appeared to be consumed by a predator. Of the thirteen PSATs prematurely released, three were released early inside Chesapeake Bay after 5 to 26 d at liberty, four have a report date, but no reported end location, and the remaining six were released en route to winter feeding grounds (Table 1). Horizontal movement patterns Based on the successful PSATs that remained on the rays for the programmed time, three female cownose rays migrated to the coast of central Florida, between Palm Bay, FL and Daytona, FL, around mid-December in 2011 (Fig. 1). Ray 4 in 2009 appeared to migrate off the coast of South Carolina, USA, and the end location for that tag transmitted in the middle of North Atlantic in the beginning of January 2010 (Fig. 2a). The end location and migration track suggested that the ray was swimming with or was caught by the Gulf Stream. Two tags that detached successfully from male rays in late November and early December (Ray 18 and 25) were also found on the coast of central Florida within the same range as the female rays. An assumption was made that the location where the tag found by the beachcomber a year after its scheduled release was close to the pop-up location. Other satellite tags attached on females and males that were deployed for shorter time periods had end locations along the southeastern coast of the United States from Virginia to Georgia (Fig. 1). In contrast to the fairly accurate end locations, the migration tracks based on the geolocations from lightlevels had large errors. With the secondary bathymetry correction, most of the estimated latitude and longitude

Environ Biol Fish

Fig. 2 Monthly geolocations and most probable tracks estimated by WC-GPE3 for four female and two male cownose rays tagged with PSATs

coordinate pairs from the programs KFTRACK and UKFSST were invalid. The WC-GPE3 program, which is based on the gridded hidden Markov model, provided plausible most-probable-tracks (Fig. 2). Most of the female rays followed similar movement patterns to one another. All the females migrated out of Chesapeake Bay immediately or soon after being tagged. These rays appeared to either stay around the mouth of the Bay or make small movements up and down the coast of Virginia until October. We considered this time period and the general vicinity as the staging time and area. For the purposes of this study, the staging area was demarcated as the area north of Cape Hatteras, North Carolina (35.255°N, 75.520°W) and south of the mouth of the Chesapeake Bay (37.06°N, 75.73°W). Most female rays left the staging area (i.e., traveled past Cape Hatteras) in early to mid-October, except Ray 4 left in early November (Table 1, Fig. 2). Based on the most-probable-tracks, the females continued a southerly, fall migration following the coastline of southeastern

United States. Although the average track followed the coastline, female rays 10 and 12 appeared to deviate from the shallower waters along the coastline to past the continental shelf into deeper waters for short periods of time according to their WC-GPE3 tracks (Fig. 2c, d). For the tags that remained attached until the scheduled release, the calculated migration rate for the female cownose rays ranged from 32.9–55.7 km/day based on the estimated geolocations and 10.0–23.9 km/day for the minimum migration rate range based on the average pathway (Table 2). The estimated most-probable-tracks from the PSATs that were released early from the rays in October through November followed the average female track. Timing of the migrations appeared to coincide with the other female rays. The tags that were released on schedule on three male rays, Rays 18, 21 and 25, provided the only informative data on wintering location and movement patterns for male rays (Table 1). The recovered tag on Ray 18 provided detailed information of the movements of the

Environ Biol Fish Table 2 Calculated migration rates for cownose ray from Cape Hatteras (exiting staging area) to the end location for each tag based on the estimated geolocations (possible rate) and an average pathway (minimum rate). Movement rate was calculated for the male rays after exiting Chesapeake Bay through summer and early fall Ray # Sex Migration rates (km/day)

Male summer movement rate Geolocations Average Pathway (km/day)

8

F

55.7

23.9

-

10

F

32.9

14.5

-

12

F

37.1

13.8

-

18

M

105.1

34.2

77.3

21

M

-

-

41.6

male ray throughout the time period. The tag on Ray 25 was only able to transmit a few messages to passing satellites; thus limited information was inferred. The third successful tag on Ray 21 only yielded a partial, fall track because the tag release date was set to midOctober. From the available tagging data, it appeared that the males migrated out of Chesapeake Bay at the end of June and July and meandered around the coast of Virginia. Around mid- to late- July, the males began a northerly migration along the coast (Fig. 2e, f). In August, the male rays with estimated geolocation tracks were most likely off the coast of Long Island, New York and Rhode Island. Ray 18 never appeared to travel farther north past Cape Cod or George’s Bank, while Ray 21 made a slightly longer migration past Cape Cod and possibly to the George’s Bank region (Fig. 2e, f). At the end of September and October, the male rays migrated back south toward the Virginia coast. The tag on Ray 21 ended in the staging area in October as discussed previously (Fig. 2f). The calculated movement rate for the northward migration patterns ranged from 41.6– 77.3 km/day based on the estimated geolocations (Table 2). This rate included migration and swimming patterns during the summer. Ray 18 continued to a southerly migration similar to the tagged female rays. Ray 25 with the limited information appeared to have two highly probable locations in which the timing and location aligned with the other males. The end positions and tracks for the two male rays were located off the coast of central Florida (Fig. 1). The Cape Hatteras to winter grounds migration rate from the estimated geolocations for Ray 18 was 105.1 km/day and a minimum of 34.2 km/day based on the average pathway

calculations (Table 2). We were not able to produce the southern migration rates for the other two male rays because the tag on Ray 21 was released prior to the southern fall migration, and the tag on Ray 25 did not provide enough information. Overall, the estimated longitudes from the tagging data followed the east coast of the United States coastline longitude track. For the female rays, the coastline longitude track began in Chesapeake Bay and continued south to central Florida. The coastline longitude track for male rays started in the Bay, demarcated the east coast longitudes in a northward direction to Rhode Island and then traced back down the coastline to central Florida. Based on the information from WC-GPE3 the female rays appeared to have followed the east United States coastline pattern for their fall migration down to the coastal waters of central Florida (Fig. 3a, b). The longitude tracks for male rays also followed the general pattern of the longitude of the east coast of the United States (Fig. 3c, d). Generally, the longitudes predicted by WCGPE3 more closely followed the coastline longitudes than the longitudinal tracks from UKFSST. Vertical movement and habitat preferences Temperature and depth records were examined from tags that were deployed for greater than 20 days. In general, male rays occupied a wider range of depths (0–51 m) compared to females (0–26 m) (Table 3, Figs. 4, 5). According to the geolocation data, male rays occupied areas that had deeper depths available, especially in August, September and October. Male cownose rays made frequent dives (3–8 per hour) throughout the summer and fall returning to shallower depths (<15 m) between dives (Fig. 6a, b). The males generally stayed closer to the surface and made repeated dives during the summer in Chesapeake Bay, while they appeared to stay closer to the substrate and returned to the surface less frequently when on the wintering grounds. The male rays spent 50% of their time during both the day and night at the surface and ~85% of the time in depths between 0 and 15 m (Fig. 5a). The males tended to prefer shallower waters (0–10 m) from June through September and slightly deeper water in November and December (Fig. 4a). Female rays, similar to the males, occupied shallower depths during September and October, but were found at deeper depths (10–25 m) a higher percentage of the time

Environ Biol Fish Fig. 3 Longitude tracks from WC-GPE3 and UKFSST programs for female cownose rays, Ray 10 (a) and 12 (b), and male cownose rays, 18 (c) and 21 (d), overlaid on longitudes of the United States eastern seaboard coastline

during November and December (Fig. 4b). The average depths (± 1 sd) in November and December (11.4 ± 4.8 and 11.5 ± 3.9 m, respectively) were deeper than the average overall depth (9.3 ± 8.8 m). However, compared to males, the female cownose rays tended to spend more time throughout 25 m and shallower in the water column (Fig. 5b). Female rays do not appear to stay at constant depths for long periods of time when migrating or when occupying their summer habitat. Similar to the males, the female rays dove less frequently when inhabiting their winter grounds (Fig. 6f).

Table 3 Mean (± standard deviation) and range (minimummaximum) depth (m) and temperature (°C) for male and female cownose rays and day and night recordings from the PSATs. Depth and temperature p-values based on linear mixed effects model with repeated measures

Depth (m) Temperature (°C)

Depth (m) Temperature (°C)

Male

Female

p-value

8.2 (± 9.5) (0–50.7) 21.9 (± 2.3) (11.9–30.1)

11.2 (± 7.1) (0–26.0) 22.6 (± 1.7) (18.6–27.2)

0.004

Day

Night

p-value

8.9 (± 8.7) (0–50.7) 22.1 (± 2.2) (12.3–28.7)

8.8 (± 9.2) (0–49.6) 22.2 (± 2.1) (13.0–30.1)

0.416

0.003

0.511

There was no diel difference in the distribution of depth for the rays in this study according to the mixed effects model (F1, 27 = 0.68, p = 0.416) and no interactions were found; however, the sex of the ray was significant (F1,33.2 = 9.76, p = 0.004; Table 3). The estimated parameters for sex and time period in the depth model were as follows: Females = 1.4 ± 0.1, Males = 1.9 ± 0.1, Day = 1.7 ± 0.1, Night = 1.6 ± 0.1. The autoregressive 1 (AR(1)) covariance structure was best for both depth and temperature models. Similar to the depth model, there were no diel differences in water temperature distribution for the rays in this study (F1, 22.8 = 0.45, p = 0.511), but the sex factor was significant (F1,23.4 = 10.61, p = 0.003; Table 3). The e s t i m a t e d p a r a m e t e r s w e r e a s f o l l ow s : F e males = 23.3 ± 0.4, Males = 21.8 ± 0.2, Day = 22.4 ± 0.26, Night = 22.6 ± 0.3. No interactions between the variables were found. The temperature range for the female cownose rays (18.6–27.2 °C) was narrower than males (11.9–30.1 °C; Table 3). This is directly related to the deeper depths to which the male rays were able to dive. From June to September, the temperature averages decreased, but the range was still large (Fig. 4c). The minimum and maximum temperatures recorded were from male rays, 11.9 °C in September, and 30.1 °C in July, respectively. In November and December, the male cownose rays stayed in slightly warmer water, which corresponded to the shallower depth profiles (Fig. 4a, c). The female cownose rays in this study stayed in warmer

Environ Biol Fish Fig. 4 Distribution of depth and temperature for each month for males (a & c) and female (b & d) cownose rays. Dashed line indicates the average temperature or depth for all rays combined (n = 18,425)

water from September through November, but preferred colder water in December compared to the males (Fig. 4a).

In both the day and night time periods, the males spend about 40–45% of their time at 21–23 °C, whereas the females spend about 35–40% of their time at that temperature range (Fig. 5c, d). The average temperature profile for all rays was 22.1 ± 2.1 °C and the majority of the recorded temperatures were from 20 to 24 °C.

Discussion

Fig. 5 Percentage of total time cownose rays spent at each depth (5 m bin-size) and temperature (1 °C bin-size) during night (grey) and day (white) time periods for male (a & c) and female (b & d) tagged rays at liberty for more than 20 days (n = 18,425)

Based on the PSAT data, we can confirm the location of the wintering grounds for cownose rays from Chesapeake Bay. Both sexes appear to aggregate around the coastal areas of central Florida between Daytona Beach and West Palm Beach, Florida. Three tags (from 2 females and 1 male) were released within an 8.5 km area of one another according to the Argos satellites. Grusha (2005) also identified central Florida as the wintering grounds for female cownose rays from Chesapeake Bay. This information revealed part of the migration pattern and confirmed overwintering grounds along the east coast of Florida as an important ecosystem for cownose rays. The general track gave reasonable large-scale movement patterns, with the possibility of some rays swimming beyond the continental shelf for short periods of time. Extended time in deeper waters does not seem likely because the rays are strongly associated with the benthic substrate for feeding. Results from the male tracks suggest that the cownose rays that inhabit Chesapeake Bay in early summer have a longer migration than the females. The tracks from two males suggest a second summer feeding area for males off the coast of southern New England post mating and are able to have faster migration rates compared to females.

Environ Biol Fish

Fig. 6 Sample of long and short time periods of diving behavior during the late summer/ early fall for male (a & b) and female (e) cownose rays and when the rays are on their wintering grounds (males: c & d; females: f)

The question remains as to why the males choose to leave and expend more energy for the long migration northward. One hypothesis is that the male cownose rays migrate out of the Bay to reduce competition for the food and habitat resources for the females and pups. Fisher (2010) suggests sex-specific differences in cownose ray foraging tactics in Chesapeake Bay during mixed sex schooling prior to mating. Females were observed to target a larger array and more nutrient rich prey than males. Chesapeake Bay has nutrient rich and easily accessible prey and offers protection from most large predators (i.e., sharks). Thus, it is advantageous for the overall population to allow females and young to stay inside the nursery grounds within the bay where it is safer and to reduce the competition for the ideal feeding habitat. Although males are subjected to more extensive migratory movement than females, post-mating habitats off New Jersey through southern New England are productive and support a large and diverse community of marine life (Georges Bank; Garrison and Link 2000). A second hypothesis is that the males are able to exploit

these other areas with high quality prey items in colder waters, whereas the females may be restricted to warmer waters for embryonic development and reduce the possible physiological stress endured from deep dives. The WC-GPE3 tracks indicated that the female cownose rays migrate from Chesapeake Bay along the coastline to their wintering grounds in central Florida during the fall. The timing of movement suggests that male rays migrate south with the females by regrouping with the schools in the general staging area. The high seasonal occurrences of rays in the coastal waters of North Carolina align with the timing when tagged rays in this study were migrating along the coast of North Carolina. Goodman et al. (2011) found higher abundances of cownose rays in the spring time and late autumn in the coastal waters during known migration periods compared to the lower group sizes inside the North Carolina estuaries in the summer. The differences in abundance during the different seasons may suggest that the spring and fall migrations include cownose rays from the entire Atlantic population. Our study suggests

Environ Biol Fish

that the Atlantic populations of cownose rays (R. bonasus) do not migrate around the southern part of Florida to the Gulf of Mexico. This finding supports the premise that the cownose rays in the Atlantic area are a separate stock from the R. bonasus in the Gulf of Mexico. Recent genetic work determined the presence of at least two distinct stocks of R. bonasus in Chesapeake Bay and Gulf of Mexico (McDowell and Fisher 2013). Likewise, cownose rays in the Gulf of Mexico are found to mature at an earlier age (age 4–5) (Neer and Thompson 2005) compared to age 6–7 and 7–8 for males and females, respectively, in Chesapeake Bay (Smith and Merriner 1987; Fisher et al. 2013). Neer and Thompson (2005) also showed that pupping occurs in mid-April through possibly November, which is much earlier and longer than in Chesapeake Bay (Fisher 2010). The differences in the pupping season are likely a result of the warmer waters in the Gulf of Mexico compared to the Atlantic. However, maturity and pupping season could potentially be confounded because there are two species of cownose rays, R. bonasus and R. brasiliensis, in the Gulf of Mexico that are difficult to distinguish from one another (J. McDowell, pers. comm.). The behavior of the cownose rays showed no differences with depth and temperature preferences during the two diel periods. However, there were differences between sexes in their profiles for mean temperature and depth throughout the seasons. Male rays occupied a broader depth range compared to females, but this was influenced by their longer migration and feeding habitat. The northern second feeding habitat for males is deeper (up to 100 m), whereas the depth in the Chesapeake Bay ranges from 0 to 53 m with an average of 6.5 m. Male dive trends suggested that males forage for benthic prey in the northern habitat, but return to shallower depths between dives possibly to reduce physiological stress. On the wintering grounds, the rays appeared to dive less frequently. This could be a result of bottom water temperatures being within preferable temperature range. Our results support their epipelagic habit; the rays spend most of their time at the surface, particularly when they are migrating. The males in this study spent half of their time at the surface (0–5 m) and 85% of their time at depths from 0 to 15 m. The females were not as associated with the surface as the males, spending only about 30% of their time

between 0 and 5 m. Females were found throughout 0–20 m from September to December. The cownose rays from Chesapeake Bay were tolerant of a wide range of temperatures, particularly the males (recorded range: 11.9–30.1 °C). According to Schwartz (1964), the lethal minimum temperature for cownose rays is about 12 °C. However, a sudden drop in temperature to 3.4 °C did not appear to distress two of the captive specimens for a short time period (Schwartz 1964). Schwartz’s study and results from this study suggest that the rays can tolerate colder waters for a short amount of time, for example, for episodic diving and feeding. Deep, short duration dives appeared to be the feeding strategy for the male rays in the northern summer grounds. In addition, tags from this study rarely recorded temperatures above 29 °C, which supports the finding that cownose rays avoided temperatures greater than 30 °C (Neer et al. 2007). Temperature and depth had no effect on the distribution of cownose rays in the Caloosahatchee River, FL (Collins et al. 2008) and along the northwestern part of the Gulf of Mexico (Craig et al. 2010). The rays studied by Craig et al. (2010) were most abundant around highly productive, riverine-influenced areas. Perhaps the cownose rays from Chesapeake Bay also seek areas that are highly productive with little regard for temperatures within a certain range. In conclusion, the rays appear to be tolerant of temperature changes within a range from 18 to 28 °C and can handle more extreme temperatures for short periods of time. The success rates and data transmitted from the deployed tags varied each year. Out of 25 PSATs deployed overall, only 7 were released and transmitted messages on schedule (28%). The non-reporting rate of the satellite tags in this study was 20% (5 out of 25 tags) and the percent of premature detachment was 52% (13 tags). These percentages align with those in the literature (Musyl et al. 2011). The reporting rate for Wildlife Computer pop-up satellite tags was calculated to be about 86% (all PSATs = 79%) with only about 18% of the reporting tags remaining attached until the programmed release (Musyl et al. 2011). Non-reporting and premature release is a common issue for PSATs. These tag failures arise from either issues with the tag or animal. Problems originating from the tag may include: battery failure, tag damage (e.g., antenna damage), mechanical failure (e.g., tethers) and biofouling of the tag (e.g., Hays et al. 2007; Musyl et al. 2011). The tag could fail to report or be released early

Environ Biol Fish

due to problems with the location of the tag attachment on the animal (i.e., infections or tissue necrosis; Hoolihan et al. 2011), entanglement with substrate or other animals, social or mating behaviors (e.g., Swimmer et al. 2006), predation from sharks, natural mortality or mortality induced from the tagging event (e.g., Musyl et al. 2009). It is difficult to determine the exact reason behind the tag failures. It is reasonable to believe that the tags that were all released prematurely in Chesapeake Bay were due to the social behavior of the rays (mating behavior), mortality induced from tagging or entanglement with the substrate. From the PSATs, we have provided greater insight on the movement patterns and habitat use of adult male and female rays from Chesapeake Bay. The rays appear to be tolerant to changes in temperatures and utilize a wide range of habitats including estuaries with low salinity and coastal waters of depths up to 50 m. There are still many unanswered questions that need to be resolved for the appropriate management of the cownose rays on the Atlantic coast of the United States. For example, do male cownose rays that mate in bays other than Chesapeake Bay mix with Chesapeake rays off Long Island and Rhode Island? Similarly, do the wintering grounds off Florida have a mixture of rays from various summering grounds? If the cownose rays continue to draw the attention of commercial shellfish farmers and recreational fishers, implications of a fishery on this elasmobranch species would need to be considered. Presented spatial patterns of cownose ray habitat use integrated with existing published cownose ray life history, age, growth and reproductive capacity information, provides management with the tools to draft policies for recreational and commercial fisheries. Of importance for future management implications are our findings of sexual segregation occurring during targeted fishing activity periods, potentially supportive of specific time or male-only fishery policies. Acknowledgements A special thanks to John Hoenig for providing partial funding for pop-up satellite archival tags and advice throughout the project. This study was made possible by haul seiner fishermen, John Dryden and George Trice, for their assistance with the collection of rays, and field support from the volunteers and students at the Virginia Institute of Marine Science. We thank Benjamin Galuardi from National Marine Fisheries Service and Heather Baer and other members at Wildlife Computers for their programming support. All work with the capture, holding, tagging and release of cownose rays was conducted under the guidelines of Institutional Animal Care and Use Committee (IACUC) protocols (IACUC-2012-07-09-8040-rafish). This

research was carried out in part under the auspices of the Cooperative Institute for Marine and Atmospheric Studies, a cooperative institute of the University of Miami and the National Oceanic and Atmospheric Administration (cooperative agreement NA15OAR4320064), Virginia Marine Resources Commission (Award Number V774310) and equipment trust funds from College of William & Mary. This paper is Contribution No. 3654 of the Virginia Institute of Marine Science, College of William & Mary.

References Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrova BN, Csaki F (eds) Proceedings of the 2nd international symposium on information theory. Publishing House of the Hungarian Academy of Sciences, Budapest, pp 268–281 Argos (2015) Argos user’s manual. Available: http://www.argossystem.org/manual/. Accessed 2015 February Basson M, Bravington MV, Hartog JR, Patterson TA (2016) Experimentally derived likelihoods for light-based geolocation. Methods Ecol Evol 7:980–989 Bigelow HB, Schroeder WC (1953) Fishes of the western north Atlantic. Part 2: sawfishes, guitarfishes, skates, rays, and chimeroids. Memoir Sears Foundation for Marine Research, Yale University Blaylock RA (1993) Distribution and abundance of cownose rays, Rhinoptera bonasus (Rhinopteridae), in lower Chesapeake Bay, Virginia. Estuaries 16:253–263 Clark M (2001) Are deepwater fisheries sustainable?- the example of orange roughy (Hoplostethus atlanticus) in New Zealand. Fish Res 51:123–135 Collins AB, Huepel MR, Hueter RE, Motta PJ (2007) Hard prey specialists or opportunistic generalists? An examination of the diet of the cownose ray, Rhinoptera bonasus. Mar Freshw Res 58:135–144 Collins AB, Huepel MR, Simpfendorfer CA (2008) Spatial distribution and long-term movement patterns of cownose rays Rhinoptera bonasus within an estuarine river. Estuar Coasts 31:1174–1183 Craig JK, Gillikin PC, Magelnicki MA, May LN (2010) Habitat use of cownose rays (Rhinoptera bonasus) in a highly productive, hypoxic continental shelf ecosystem. Fish Oceanogr 19:301–317 Fisher RA (2009) Regional workshop on cownose ray issues identifying research and extension needs (proceedings). VIMS Marine Resource Report 2009-6. VSG-09-06 http://web.vims.edu/GreyLit/VIMS/mrr09-06.pdf Fisher RA (2010) Life history, trophic ecology & prey handling by cownose ray, Rhinoptera bonasus, from Chesapeake Bay. NOAA final report (NA07NMF4570324) Grant No. 713031. VIMS Marine Resource Report No. 2010-20, VSG-10-25 Fisher RA, Call GC, Grubbs RD (2011) Cownose ray (Rhinoptera bonasus) predation relative to bivalve ontogeny. J Shellfish Res 30:187–196

Environ Biol Fish Fisher RA, Call GC, Grubbs RD (2013) Age, growth, and reproductive biology of cownose rays in Chesapeake Bay. Mar Coast Fish: Dyn Manage Ecosyst Sci 5:224–235 Fisher RA, Call GC, McDowell JM (2014) Reproductive variations in cownose rays (Rhinoptera bonasus) from Chesapeake Bay. Environ Biol Fish 97:1031–1038 Franke E, Bade L, Curtis T, Ferrier D, Fisher R, Grubbs R, Ihde T, McDowell J, Ogburn M, Townsend H (2016) Cownose rays in the Chesapeake Bay: what do we know? Workshop report. Chesapeake bay Program, sustainable fisheries goal implementation team. Annapolis pp 1-30. http://www. chesapeakebay.net/channel_files/23141/cnr_workshop_ report_final_1-29-16.pdf Galuardi B, Royer F, Golet W, Logan J, Neilson J, Lutcavage M (2010) Complex migration routes of Atlantic bluefin tuna (Thunnus thynnus) question current population structure paradigm. Can J Fish Aquat Sci 67:966–976 Garrison LP, Link JS (2000) Fishing effects on spatial distribution and trophic guild structure of the fish community in the Georges Bank region. ICES J Mar Sci 57:723–730 Goodman MA, Conn PB, Fitzpatrick E (2011) Seasonal occurrence of Cownose rays (Rhinoptera bonasus) in North Carolina’s estuarine and coastal waters. Estuar Coasts 34: 640–651 Grubbs RD, Carlson JK, Romine JG, Curtis TH, McElroy WD, McCandless CT, Cotton CF, Musick JA (2016) Critical assessment and ramifications of a purported marine trophic cascade. Sci Rep 6:20970 Grusha DS (2005) Investigations into the life history of the Cownose ray, Rhinoptera bonasus, (Mitchill, 1815). Master’s thesis. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point Grusha DS, Patterson MR (2005) Quantification of drag and lift imiposed by pop-up satellite archival tags and estimation of the metabolic cost to cownose rays (Rhinoptera bonasus). Fish Bull 103:63–70 Harvey AC (1990) Forecasting, structural time series models, and the Kalman filter. Cambridge University Press, Cambridge Hays GC, Bradshaw CJA, James MC, Lovell P, Sims DW (2007) Why do Argos satellite tags deployed on marine animals stop transmitting? J Exp Mar Biol Ecol 349:52–60 Hill RD (1994) Theory of geolocation by light levels. In Elephant Seals: Population Ecology, Behavior, and Physiology. In: Boeuf L, Burney J, Laws RM (eds) . University of California Press, Berkeley, pp 227–236 Hoenig JM, Gruber SH (1990) Life-history patterns in the elasmobranchs: implications for fisheries management. In: HL Pratt, SH Gruber, T Taniuchi (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics and the status of the fisheries. NOAA Technical Report 90:1–16. U.S. Dept. Comm., Washington, DC Hoolihan JP (2005) Horizontal and vertical movements of sailfish (Istiophorus platypterus) in the Arabian gulf, determined by ultrasonic and pop-up satellite tagging. Mar Biol 146:1015– 1029 Hoolihan JP, Luo J, Abascal FJ, Campana SE, De Metrio G, Dewar H et al (2011) Evaluating post-release behaviour modification in large pelagic fish deployed with pop-up satellite archival tags. ICES J Mar Sci: Journal du Conseil 68:880–889

Lam CH, Nielsen A, Sibert JR (2008) Improving light and temperature based geolocation by unscented Kalman filtering. Fish Res 91:15–25 Le Port A, Sippel T, Montgomery JC (2008) Observation of mesoscale movements in the short-tailed stingray, Dasyatis brevicaudata, from New Zealand using a novel PSAT tag attachment method. J Exp Mar Biol Ecol 359:110–117 Luckenbach MW, Coen LD, Ross PG Jr, Stephen JA (2005) Oyster reef habitat restoration: relationships between oyster abundance and community development based on two studies in Virginia and South Carolina. J Coast Res 40:64–78 McDowell JR, Fisher RA (2013) Discrimination of cownose ray, Rhinoptera bonasus, stocks based on microsatellite DNA markers. NOAA final report (NA11NMF4570215), VIMS Marine Resource Report No. 2013-8 McEachran JD, Fechhelm JD (1998) Fishes of the Gulf of Mexico, vol 1. University of Texas Press, Austin Merriner JV, Smith JW (1979) A report to the oyster industry of Virginia on the biology and management of the Cownose ray (Rhinoptera bonasus, Mitchill) in lower Chesapeake Bay. Virginia Institute of Marine Science, Special report in applied marine science and ocean engineering 216, Gloucester point Murray TJ, Hudson K (2015) Virginia shellfish aquaculture situation and outlook report: results of the 2014 Virginia shellfish aquaculture crop reporting survey. VIMS Marine Resource Report 2015-3. VSG-15-01 Musick JA (1999) Life in the slow lane: ecology and conservation of long-lived marine animals. Am Fish Soc Symp 23:1-10 Musyl MK, Brill RW, Curran DS, Gunn JS, Hartog JR, Hill RD et al (2001) Ability of archival tags to provide estimates of geographical position based on light intensity. In: Sibert J, Nielsen J (eds) Electronic tagging and tracking in marine fisheries reviews: methods and technology in fish and biology and fisheries. Kluwer, Dordrecht, pp 343–367 Musyl MK, Moyes CD, Brill RW, Fragoso NM (2009) Factors influencing mortality estimates in post-release survival studies. Mar Ecol Prog Ser 396:157–159 Musyl MK, Domeier ML, Nasby-Lucas N, Brill RW, McNaughton LM, Swimmer JY, Lutcavage MS, Wilson SG, Galuardi B, Liddle JB (2011) Performance of pop-up satellite archival tags. Mar Ecol-Prog Ser 433:1–28 Neer JA, Thompson BA (2005) Life history of the cownose ray, Rhinoptera bonasus, in the northern Gulf of Mexico, with comments on geographic variability in life history traits. Environ Biol Fish 73:321–331 Neer JA, Rose KA, Cortes E (2007) Simulating the effects of temperature on individual and population growth of Rhinoptera bonasus: a coupled bioenergetics and matrix modeling approach. Mar Ecol-Prog Ser 329:211–223 Paolisso M, Dery N, Herman S (2006) Restoration of the Chesapeake Bay using a non-native oyster: ecological and fishery considerations. Hum Organ 65:253–267 Peterson CH, Fodrie FJ, Summerson HC, Powers SP (2001) Sitespecific and density-dependent extinction of prey by schooling rays: generation of a population sink in top-quality habitat for bay scallops. Oecologia 129:349–356 R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN: 3–900051–08-9, URL: http://www.R-project.org/ Rogers C, Roden C, Lohoefener R, Mullin K, Hoggard W (1990) Behavior, distribution, and relative abundance of cownose

Environ Biol Fish ray schools Rhinoptera bonasus in the northern Gulf of Mexico. NE Gulf Sci 11:69–76 Schwartz FJ (1964) Effects of winter water conditions on fifteen species of captive marine fishes. Am Midl Nat 71:434–444 Sibert JR, Musyl MK, Brill RW (2003) Horizontal movements of bigeye tuna (Thunnus obesus) near Hawaii determined by Kalman filter analysis of archival tagging data. Fish Oceanogr 12:141–151 Smith JW, Merriner JV (1985) Food habits and feeding behavior of the Cownose ray, Rhinoptera bonasus, in lower Chesapeake Bay. Estuaries 8:305–310

Smith JW, Merriner JV (1986) Observations on the reproductive biology of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay. U.S. NMFS Fish Bull 84:871–877 Smith JW, Merriner JV (1987) Age and growth, movements and distribution of the Cownose ray, Rhinoptera bonasus, in Chesapeake Bay. Estuaries 10:153–164 Swimmer Y, Arauz R, McCracken M, McNaughton L, Ballestero J, Musyl M et al (2006) Diving behavior and delayed mortality of olive ridely sea turtles Lepidochelys olivacea after their release from longline fishing gear. Mar Ecol-Prog Ser 323:253–261 Teo SL, Boustany AM, Block BA (2007) Oceanographic preferences of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Mar Biol 152:1105–1119