Multi-Year Movements of Adult and Subadult Bull Sharks (Carcharhinus Leucas): Philopatry, Connectivity, and Environmental Influences
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Aquat Ecol https://doi.org/10.1007/s10452-021-09845-6 (0123456789().,-volV)( 0123456789().,-volV) Multi-year movements of adult and subadult bull sharks (Carcharhinus leucas): philopatry, connectivity, and environmental influences Mitchell J. Rider . Laura H. McDonnell . Neil Hammerschlag Received: 9 December 2020 / Accepted: 20 February 2021 Ó The Author(s), under exclusive licence to Springer Nature B.V. 2021 Abstract Understanding the movement ecology of Biscayne Bay during the colder dry season (November marine species is important for conservation manage- to February) and lower residencies during the warmer ment and monitoring their responses to environmental wet season (June to October). These seasonal patterns change. In this study, adult and subadult bull sharks were supported by catch data from long-term fishery- (Carcharhinus leucas; n = 16) were acoustically independent shark surveys in the study area. During tagged in Biscayne Bay, Florida (USA), where they summer months when residencies of C. leucas were tracked locally via an array of 40 passive acoustic declined in Biscayne Bay, their residencies increased receivers, as well as regionally via cooperative in other regions (e.g., Florida Gulf Coast), demon- acoustic telemetry networks, with individuals tracked strative of seasonal migrations. Connectivity between up to 4.5 years. Detection data were used to assess areas of high use (Biscayne Bay and Florida Gulf philopatry, regional connectivity, and environmental Coast) was demonstrated by some individuals travel- correlates of shark habitat use. Spatial range varied per ing between these areas. Results from generalized individual; however, most individuals displayed high additive mixed models suggest that these movement residency to Biscayne Bay, exhibiting strong philopa- patterns could be partially driven by seasonal changes tric behavior to the tagging area. A generalized linear in environmental variables as well as an individual’s mixed model revealed a seasonal pattern in habitat life stage, including reproductive status. use, with mature females displaying high residency in Keywords Movement ecology Á Acoustic telemetry Á Philopatry Á Tracking Á Highly migratory Handling Editor: Te´lesphore Sime-Ngando species Á Carcharhinus leucas Supplementary information The online version contains supplementary material available at (https://doi.org/10.1007/ s10452-021-09845-6) Introduction M. J. Rider (&) Á L. H. McDonnell Á N. Hammerschlag Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA Determining the spatial ranges and movement patterns e-mail: [email protected] of mobile species is critical for conservation manage- ment, including establishing effective place-based L. H. McDonnell Á N. Hammerschlag management (Hays et al. 2019) and predicting species Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, Coral Gables, responses to environmental change (Birkmanis et al. FL, USA 123 Aquat Ecol 2020; Niella et al. 2020). This is particularly important grounds along the U.S. eastern seaboard due to for threatened and vulnerable species, where an warming (Bangley et al. 2018), suggesting the possi- understanding of their spatial use can inform effective bility of range shifts in adults due to climate change. spatial protections (Knip et al. 2012; Graham et al. Therefore, there is a need to further examine move- 2016; McDonnell et al. 2020), enable population ment patterns of adult and subadult life stages of C. recovery (Speed et al. 2018), and track their responses leucas over longer time periods (i.e., years) to to climate change (Birkmanis et al. 2020). Under- determine potential philopatric behavior to specific standing habitat use and residency patterns can shed locations, possible regional connectivity, and if and light on both short- and long-term space use and may how changes in environmental conditions, particularly even highlight differences in environmental prefer- temperature, influence these movement patterns. ences (Bangley et al. 2020), social networks (Jacoby Acoustic telemetry has been previously used to et al. 2016), foraging behaviors (Bailey et al. 2012), track long-term movements of adult C. leucas, for and predator–prey interactions (Hammerschlag et al. example in South Africa and Australia, pinpointing 2012). important aggregation sites, highlighting seasonal Studying the movements of highly migratory residency patterns (Daly et al. 2014), and even species within the marine environment is inherently predicting responses to environmental change (Niella challenging, as it can be difficult to differentiate et al. 2020). Moreover, the rise in cooperative acoustic between populations and to delineate precise residen- telemetry networks permits researchers to track their cies and areas of core use. Over the last decade, acoustically tagged animals outside of their own however, advances in biotelemetry have enabled arrays, enabling them to answer important research researchers to more effectively remotely track the questions over a wider spatial scale (Crossin et al. movements of wide-ranging marine animals, such as 2017; Friess et al. 2020; Bangley et al. 2020). These large sharks (Cooke 2008; Hammerschlag et al. 2011; networks and their associated data-sharing policies Hussey et al. 2015). These technologies have allowed can facilitate the examination of movement patterns of marine scientists to determine specific movement wide-ranging demersal species, like C. leucas over metrics, including spatial range, connectivity, and larger spatial and temporal scales. activity levels (e.g., Howey-Jordan et al. 2013; In this study, we used passive acoustic telemetry Guttridge et al. 2017; Skubel et al. 2020). data to investigate potential philopatric behavior, Bull sharks (Carcharhinus leucas) are large marine regional connectivity, and environmental correlates predators that occupy tropical and warm temperate of habitat use by adult and subadult C. leucas tagged in waters around the globe (Castro 2010). To date, most Biscayne Bay (Florida). Spanning multiple years of movement studies of this species within U.S. waters tracking (up to 4.5 years), acoustic detection data were have focused on juvenile life stages within specific obtained through our own local array in Biscayne Bay nursery areas (e.g., Simpfendorfer et al. 2005; Ortega and from four cooperative acoustic tracking networks et al. 2009; Curtis et al. 2011; Drymon et al. 2013), covering coastal areas of the U.S. eastern seaboard and with only a few evaluating habitat use of adult and Gulf of Mexico. These data were supplemented with subadult life stages (e.g., Carlson et al. 2010; Ham- fishery-independent shark abundance surveys in Bis- merschlag et al. 2012). Such studies have generally cayne Bay. We used these data to address the revealed preference for shallow (\ 20 m) and warm following three questions: (1) What is the spatial (26 °C–33 °C) coastal waters by mature and maturing extent of C. leucas tagged in Biscayne Bay to other C. leucas, largely restricted to inshore areas, with coastal regions covered by acoustic receivers within relatively low mobility. These findings have implica- the U.S. Atlantic and Gulf of Mexico? (2) What role do tions for conservation and management of adults as the these regions serve in C. leucas’ seasonal migrations core use areas of tagged individuals have rarely (end point or pathway), and is there any evidence of spanned multiple jurisdictions (Graham et al. 2016; philopatric behavior within any of them? (3) Do any Calich et al. 2018). However, tracking periods of these relationships exist between key environmental vari- previous studies were relatively short (median track- ables measured within regions and the number of days ing periods less than 3 months). Additionally, recent C. leucas were detected there per month? evidence indicates poleward shifts in C. leucas nursery 123 Aquat Ecol Methods Study site Study species All C. leucas individuals considered for this study were originally caught in Biscayne Bay, Florida. This Bull sharks (Carcharhinus leucas) are common to bay is a clear water barrier island lagoon that spans the tropical and subtropical coastal waters. Along the At- coastline from the city of Miami to the beginning of lantic Coast of the United States, they range from the Florida Keys (* 56 km by * 13 km). It is Massachusetts to the Gulf of Mexico (Castro 2010). primarily a benthic-based ecosystem containing com- Among the top marine predators in South Florida munities of seagrasses and corals and is also charac- waters (Shipley et al. 2019), C. leucas consumes a terized by areas of estuarine habitats (Browder et al. wide variety of fishes and small elasmobranchs and 2005), similar to those known to attract C. leucas at occurs in considerably high numbers during the winter younger life stages (Wiley and Simpfendorfer 2007). and spring (Castro 2010). The northern part of Biscayne Bay borders the city of These sharks are born at approximately 60 cm– Miami, subjecting waters in this area to effects of 75 cm total length (TL) (Branstetter and Stiles 1987) urbanization, including but not limited to chemical and use inshore estuaries as nursery areas as juveniles and noise pollution, coastal development, and a high until reaching approximately 190 cm TL (Curtis et al. level of human recreation (Rider 2020). 2011), after which they expand their range to adjacent In Biscayne Bay, an array consisting of 40 Inno- coastal areas