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An assessment of juvenile sand tiger (Carcharias taurus) activity patterns in a seasonal nursery using accelerometer transmitters

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Abstract

Telemetry transmitters incorporating accelerometers have recently emerged as powerful tools for investigating the activity patterns of individuals and groups of individuals in nearshore environments. Data obtained from these devices provide not only a time series of animal occurrence at acoustic receivers, but also a direct measure of animal activity, which can be used to quantify trends in activity states over time and in relation to exogenous factors. Here we used passive acoustic accelerometry to examine trends in the activity and swimming depth of eight juvenile sand tigers (Carcharias taurus) in Plymouth, Kingston, Duxbury (PKD) Bay, Massachusetts, USA, a recently identified nursery area. We applied a novel geostatistical modeling approach that accounts for both latent spatial and individual variation to assess the effects of time of day, tidal stage, water temperature, and lunar phase on activity patterns at both a population- and individual-level. The best-fitting model indicated that juvenile sand tigers were more active and more likely to be detected at the surface at night and during the new moon; water temperature was also a predictor of surface activity. Collectively, our results confirm conventional wisdom that sand tigers are slow-moving fish that are more active at night and provide evidence that high activity in PKD Bay may be indicative of foraging activity.

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References

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In Petrov BN, Csaki F (eds) Second international symposium on information theory. Budapest, Hungary pp 267–281

  • ASMFC (Atlantic States Marine Fisheries Commission) (2008) Interstate fishery management plan for Atlantic coastal sharks. ASMFC, Washington, DC 172pp

    Google Scholar 

  • Barnett A, Payne NL, Semmens JM, Fitzpatrick R (2016) Ecotourism increases the field metabolic rate of whitetip reef sharks. Biol Conserv 199:132–136

    Article  Google Scholar 

  • Beck MW, Heck KL Jr, Able KW, Childers DL, Eggleston DB, Gillanders BM et al (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51(8):633–641

    Article  Google Scholar 

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

    Google Scholar 

  • Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. Fish Bull 53:74

    Google Scholar 

  • Brewster LR, Dale JJ, Guttridge TL, Gruber SH, Hansell AC, Elliott M, Cowx IG, Whitney NM, Gleiss AC (2018) Development and application of a machine learning algorithm for classification of elasmobranch behaviour from accelerometry data. Mar Biol 165(4):62

    Article  CAS  Google Scholar 

  • Brodie S, Taylor MD, Smith JA, Suthers IM, Gray CA, Payne NL (2016) Improving consumption rate estimates by incorporating wild activity into a bioenergetics model. Ecol Evol 6(8):2262–2274

    Article  Google Scholar 

  • Brownscombe JW, Wilson AD, Samson E, Nowell L, Cooke SJ, Danylchuk AJ (2015) Individual differences in activity and habitat selection of juvenile queen conch evaluated using acceleration biologgers. Endanger Species Res 27(2):181–188

    Article  Google Scholar 

  • Brownscombe JW, Cooke SJ, Danylchuk AJ (2017) Spatiotemporal drivers of energy expenditure in a coastal marine fish. Oecologia 183(3):689–699

    Article  Google Scholar 

  • Bruce BD, Stevens JD, Bradford R (2005) Designing protected areas for grey nurse sharks off eastern Australia (p. 56). Hobart: CSIRO Marine and Atmospheric Research

  • Burnett NJ, Hinch SG, Donaldson MR, Furey NB, Patterson DA, Roscoe DW, Cooke SJ (2014) Alterations to dam-spill discharge influence sex-specific activity, behaviour and passage success of migrating adult sockeye salmon. Ecohydrology 7(4):1094–1104

    Google Scholar 

  • Carlson JK, McCandless C, Cortés E, Grubbs RD, Andrews KI,. MacNeil MA, Musick JA (2009) An update on the status of the sand tiger shark, Carcharias taurus, in the Northwest Atlantic Ocean. NOAA Tech Memorandum NMFS-SEFSC-585

  • Castro J, Woodley CM, Brudeck R (1999) A preliminary evaluation of the status of shark species. FAO Fisheries Technical Paper No. 380, FAO, Rome, 72pp

  • Collette BB, Klein-MacPhee G (2002) Fishes of the Gulf of Maine, 3rd edn. Smithsonian Institute Press, Washington, DC, pp 25–27

    Google Scholar 

  • Compagno LJV (2001) Sharks of the World. FAO species catalogue for fishery purposes, No 1, vol 2. Food and Agriculture Organization of the United Nations, Rome 269 pp

    Google Scholar 

  • Gilmore RG, Dodrill JW, Linley PA (1983) Embryonic development of the sand tiger shark Odontaspis taurus (Rafinesque). Fish Bull 81:201–225

    Google Scholar 

  • Gleiss AC, Dale JJ, Holland KN, Wilson RP (2010) Accelerating estimates of activity-specific metabolic rate in fishes: testing the applicability of acceleration data-loggers. J Exp Mar Bio Ecol 385(1–2):85–91

    Article  Google Scholar 

  • Gleiss AC, Wilson RP, Shepard EL (2011) Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods Ecol Evol 2(1):23–33

    Article  Google Scholar 

  • Gleiss AC, Morgan DL, Whitty JM, Keleher JJ, Fossette S, Hays GC (2017) Are vertical migrations driven by circadian behaviour? Decoupling of activity and depth use in a large riverine elasmobranch, the freshwater sawfish (Pristis pristis). Hydrobiologia 787(1):181–191

    Article  Google Scholar 

  • Hamilton SL, Smith JE, Price NN, Sandin SA (2014) Quantifying patterns of fish herbivory on Palmyra atoll (USA), an uninhabited predator-dominated Central Pacific coral reef. Mar Ecol Prog Ser 501:141–155

    Article  Google Scholar 

  • Heithaus MR (2007) Nursery areas as essential shark habitats: a theoretical perspective. In: McCandless CT, Kohler NE, Pratt HL Jr (eds) Shark nursery grounds of the Gulf of Mexico and east coast waters of the United States. American Fisheries Society, Bethesda, MD, p 3–13.

  • Henderson MJ, Fabrizio MC, Lucy JA (2014) Movement patterns of summer flounder near an artificial reef: effects of fish size and environmental cues. Fish Res 153:1–8

    Article  Google Scholar 

  • Heupel MR, Semmens JM, Hobday AJ (2006) Automated acoustic tracking of aquatic animals: scales, design, and deployment of listening station arrays. Mar Freshw Res 57:1013–1020

    Article  Google Scholar 

  • Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297

    Article  Google Scholar 

  • Iwanowicz HR, Anderson RD, Ketschke BA (1974) A study of the marine resources of Plymouth, Kingston, and Duxbury Bay. Monograph Series Number 17. Division of Marine Fisheries, Boston, p 37

    Google Scholar 

  • Kahle D, Wickham H (2013) ggmap: spatial visualization with ggplot2. R J 5(1):144–161

  • Kneebone J, Chisholm J, Skomal GB (2012) Seasonal residency, habitat use, and site fidelity of juvenile sand tigers Carcharias taurus in a Massachusetts estuary. Mar Ecol Prog Ser 471:165–185

    Article  Google Scholar 

  • Kneebone J, Chisholm J, Bernal D, Skomal GB (2013) The physiological effects of capture stress, recovery, and post-release survivorship of juvenile sand tigers (Carcharias taurus) caught on rod and reel. Fish Res 147:103–114

    Article  Google Scholar 

  • Kneebone J, Chisholm J, Skomal G (2014) Movement patterns of juvenile sand tigers (Carcharias taurus) along the east coast of the USA. Mar Biol 161(5):1149–1163

    Article  Google Scholar 

  • Knip DM, Heupel MR, Simpfendorfer CA (2010) Sharks in nearshore environments: models, importance, and consequences. Mar Ecol Prog Ser 402:1–11

    Article  Google Scholar 

  • Kolarevic J, Aas-Hansen Ø, Espmark Å, Baeverfjord G, Terjesen BF, Damsgård B (2016) The use of acoustic acceleration transmitter tags for monitoring of Atlantic salmon swimming activity in recirculating aquaculture systems (RAS). Aquac Eng 72:30–39

    Article  Google Scholar 

  • Kristensen K, Nielsen A, Berg CW, Skaug H, Bell BM (2016) TMB: automatic differentiation and Laplace approximation. J Stat Softw 70:1–21

    Article  Google Scholar 

  • Lazaridis E (2014) Lunar: lunar phase & distance, seasons and other environmental factors (version 0.1-04). Available from http://statistics.lazaridis.eu

  • Lear KO, Whitney NM, Brewster LR, Morris JJ, Hueter RE, Gleiss AC (2016) Correlations of metabolic rate and body acceleration in three species of coastal sharks under contrasting temperature regimes. J Exp Biol 220:397–407

    Article  Google Scholar 

  • McKellar AE, Langrock R, Walters JR, Kesler DC (2015) Using mixed hidden Markov models to examine behavioral states in a cooperatively breeding bird. Behav Ecol 26(1):148–157

    Article  Google Scholar 

  • Lindgren F, Rue H (2015) Bayesian spatial modelling with R-INLA. J Stat Softw 63:1–25

    Article  Google Scholar 

  • Lindgren F, Rue H, Lindstrӧm J (2011) An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J R Stat Soc Ser B Stat Methodol 73:423–498

    Article  Google Scholar 

  • McLusky DS, Elliott M (2004) The estuarine ecosystem: ecology, threats and management. 3rd Edition. Oxford University Press

  • Murchie KJ, Cooke SJ, Danylchuk AJ, Suski CD (2011) Estimates of field activity and metabolic rates of bonefish (Albula vulpes) in coastal marine habitats using acoustic tri-axial accelerometer transmitters and intermittent-flow respirometry. J Exp Mar Biol Ecol 396(2):147–155

    Article  Google Scholar 

  • Musick JA, Branstetter S, Colvocoresses JA (1993) Trends in shark abundance from 1974 to 1991 for the Chesapeake bight region of the U.S. mid-Atlantic Coast. NOAA Technical Report NMFS 115

  • Musick JA, Harbin MM, Berkeley SA, Burgess GH, Eklund AM, Findley L, Gilmore RG, Golden JT, Ha DS, Huntsman GR, McGovern JC, Parker SJ, Poss SG, Sala E, Schmidt TW, Sedberry GR, Weeks H, Wright SG (2000) Marine, estuarine, and diadromous fish stocks at risk of extinction in North America. Fisheries 25:6–30

    Google Scholar 

  • NMFS (National Marine Fisheries Service) (1999) Final fishery management plan for Atlantic tunas, swordfish, and sharks. DOC/NOAA/NMFS HMS Management Division, Silver Spring, MD.

  • NMFS (National Marine Fisheries Service) (2017) Amendment 10 to the 2006 consolidated Atlantic highly migratory species fishery management plan: essential fish habitat and environmental assessment. NOAA/NMFS HMS Management Division, Silver Spring

    Google Scholar 

  • O’Toole AC, Murchie KJ, Pullen C, Hanson KC, Suski CD, Danylchuk AJ, Cooke SJ (2010) Locomotory activity and depth distribution of adult great barracuda (Sphyraena barracuda) in Bahamian coastal habitats determined using acceleration and pressure biotelemetry transmitters. Mar Freshw Res 61(12):1446–1456

    Article  Google Scholar 

  • Otway NM, Burke AL, Morrison NS, Parker PC (2003) Monitoring and identification of NSW critical habitat sites for conservation of grey nurse sharks. NSW Fish Final Rep Ser 47

  • Otway NM, Ellis MT (2011) Pop-up archival satellite tagging of Carcharias taurus: movements and depth/temperature-related use of south-eastern Australian waters. Mar Freshw Res 62:607–620

    Article  CAS  Google Scholar 

  • Papastamatiou YP, Watanabe YY, Bradley D, Dee LE, Weng K, Lowe CG, Caselle JE (2015) Drivers of daily routines in an ectothermic marine predator: hunt warm, rest warmer? PLoS One 10(6):e0127807

    Article  Google Scholar 

  • Payne NL, Gillanders BM, Webber DM, Semmens JM (2010) Interpreting diel activity patterns from acoustic telemetry: the need for controls. Mar Ecol Prog Ser 419:295–301

    Article  Google Scholar 

  • Payne NL, Smith JA, Meulen DE, Taylor MD, Watanabe YY, Takahashi A et al (2016) Temperature dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance. Funct Ecol 30(6):903–912

    Article  Google Scholar 

  • Pedersen MW, Patterson TA, Thygesen UH, Madsen H (2011) Estimating animal behavior and residency from movement data. Oikos 120:1281–1290

    Article  Google Scholar 

  • Pedersen MW, Weng KC (2013) Estimating individual animal movement from observation networks. Methods Ecol Evol 4(10):920–929

    Google Scholar 

  • Pincock, DG (2012) False detections: what are they and how to remove them from detection data. Vemco Document #: DOC-004691 Version 03

  • Pollard DA, Lincoln Smith MP, Smith AK (1996) The biology and conservation status of the grey nurse shark (Carcharias taurus Rafinesque 1810) in New South Wales, Australia. Aquat Conserv Mar Freshwat Ecosyst 6(1):1–20

    Article  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Reebs SG (2002) Plasticity of diel and circadian activity rhythms in fishes. Rev Fish Biol Fish 12(4):349–371

    Article  Google Scholar 

  • Robbins WD, Peddemors VM, Broadhurst MK, Gray CA (2013) Hooked on fishing? Recreational angling interactions with the critically endangered grey nurse shark Carcharias taurus in eastern Australia. Endanger Species Res 21(2):161–170

    Article  Google Scholar 

  • Schlaff AM, Heupel MR, Simpfendorfer CA (2014) Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review. Rev Fish Biol Fish 24:1089–1103

    Article  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464

    Article  Google Scholar 

  • Simpfendorfer CA, Yeiser BG, Wiley TR, Poulakis GR, Stevens PW (2011) Environmental influences on the spatial ecology of juvenile smalltooth sawfish (Pristis pectinata): results from acoustic monitoring. PLoS One 6(2):e16918

    Article  CAS  Google Scholar 

  • Smale MJ (2005) The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the eastern cape, South Africa. Afr J Mar Sci 27(1):331–335

    Article  Google Scholar 

  • Smale MJ, Booth AJ, Farquhar MR, Meÿer MR, Rochat L (2012) Migration and habitat use of formerly captive and wild raggedtooth sharks (Carcharias taurus) on the southeast coast of South Africa. Mar Biol Res 8:115–128

    Article  Google Scholar 

  • Smith KR, Scarpaci C, Louden BM, Otway NM (2015) Behaviour of aggregated grey nurse sharks Carcharias taurus off eastern Australia: similarities and differences among life-history stages and sites. Endanger Species Res 27(1):69–85

    Article  Google Scholar 

  • Stehfest KM, Lyle JM, Semmens JM (2015) The use of acoustic accelerometer tags to determine seasonal changes in activity and catchability of a recreationally caught marine teleost. ICES J Mar Sci 72(8):2512–2520

    Article  Google Scholar 

  • Taylor MD, McPhan L, van der Meulen DE, Gray CA, Payne NL (2013) Interactive drivers of activity in a free-ranging estuarine predator. PLoS One 8(11):e80962

    Article  Google Scholar 

  • Teter SM, Wetherbee BM, Fox DA, Lam CH, Kiefer DA, Shivji M (2015) Migratory patterns and habitat use of the sand tiger shark (Carcharias taurus) in the western North Atlantic. Mar Freshw Res 66(2):158–169

    Article  Google Scholar 

  • Thorson JT, Shelton AO, Ward EJ, Skaug HJ (2015) Geostatistical delta-generalized linear mixed models improve precision for abundance indices for west coast groundfishes. ICES J Mar Sci 72:1297–1310

    Article  Google Scholar 

  • Thorson JT, Ianelli JN, Kotwicki S (2017) The relative influence of temperature and size-structure on fish distribution shifts: a case-study on walleye Pollock in the Bering Sea. Fish Fish 2017:1–12

    Google Scholar 

  • Ubeda AJ, Simpfendorfer CA, Heupel MR (2009) Movements of bonnetheads, Sphyrna tiburo, as a response to salinity change in a Florida estuary. Environ Biol Fish 84:293–303

    Article  Google Scholar 

  • Watanuki Y, Niizuma Y, Geir WG, Sato K, Naito Y (2003) Stroke and glide of wing–propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth. Proc R Soc Lond B 270(1514):483–488

    Article  Google Scholar 

  • Watsky M, Gruber SH (1990) Induction and duration of tonic immobility in the lemon shark Negaprion brevirostris. Fish Physiol Biochem 8:207–210

    Article  CAS  Google Scholar 

  • Weltz K, Kock AA, Winker H, Attwood C, Sikweyiya M (2013) The influence of environmental variables on the presence of white sharks, Carcharodon carcharias, at two popular Cape Town bathing beaches: a generalized additive mixed model. PLoS ONE 8(7):e68554

    Article  CAS  Google Scholar 

  • Whitney NM, Papastamatiou YP, Holland KN, Lowe CG (2007) Use of an acceleration data logger to measure diel activity patterns in captive whitetip reef sharks, Triaenodon obesus. Aquat Living Resour 20(4):299–305

    Article  Google Scholar 

  • Whitney NM, Pratt HL Jr, Pratt TC, Carrier JC (2010) Identifying shark mating behaviour using three-dimensional acceleration loggers. Endanger Species Res 10:71–82

    Article  Google Scholar 

  • Whitney NM, Papastamatiou YP, Gleiss AC (2012) Integrative multi-sensor tagging: emerging techniques to link elasmobranch behavior, physiology and ecology. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives, 2nd edn. CRC Press, Boca Raton, p 265–290

  • Wilson SM, Hinch SG, Eliason EJ, Farrell AP, Cooke SJ (2013) Calibrating acoustic acceleration transmitters for estimating energy use by wild adult Pacific salmon. Comp Biochem Physiol A Mol Integr Physiol 164(3):491–498

    Article  CAS  Google Scholar 

  • Wilson SM, Hinch SG, Drenner SM, Martins EG, Furey NB, Patterson DA, Welch DW, Cooke SJ (2014) Coastal marine and in-river migration behaviour of adult sockeye salmon en route to spawning grounds. Mar Ecol Prog Ser 496:71–84

    Article  Google Scholar 

  • Winton MV, Fay G, Haas HL, Arendt M, Barco S, James MC, Sasso C, Smolowitz R (2018) Estimating the distribution and relative density of satellite-tagged loggerhead sea turtles using geostatistical mixed effects model. Mar Ecol Prog Ser 586:217–232

    Article  Google Scholar 

  • Zhu L, Li L, Liang Z (2009) Comparison of six statistical approaches in the selection of appropriate fish growth models. Chin J Oceanol Limnol 27:457–467

    Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge Pine duBois and Alex Mansfield of the Jones River Environmental Heritage Center for providing the infrastructure for our holding tank and their logistical support, Barbara Bailey and Holly Bourbon for their assistance with the holding tank construction, Jay Hilliard and Dave Lindamood for enabling the initial documentation of sharks in PKD Bay, Donald Beers and the Duxbury Harbormaster’s Office for providing dockage, and Heather Hollema for her assistance with tagging and receiver maintenance. This research was funded by awards from the NOAA Proactive Conservation Program, the Sea World Conservation Society, and the Massachusetts Environmental Trust as well as support from the Federal Aid in Sportfish Restoration Act. This is Massachusetts Division of Marine Fisheries Contribution No. 99.

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Kneebone, J., Winton, M., Danylchuk, A. et al. An assessment of juvenile sand tiger (Carcharias taurus) activity patterns in a seasonal nursery using accelerometer transmitters. Environ Biol Fish 101, 1739–1756 (2018). https://doi.org/10.1007/s10641-018-0821-4

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