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RESEARCH ARTICLE
Contents Vol 74(16)

Ontogenetic habitat partitioning among four shark species within a nursery ground

Daniel P. Crear https://orcid.org/0000-0002-9045-3649 A E * , Cassidy D. Peterson https://orcid.org/0000-0002-0836-3039 B , Jeremy M. Higgs https://orcid.org/0000-0002-7669-5529 C , Jill M. Hendon https://orcid.org/0000-0002-8339-5532 C and Eric R. Hoffmayer https://orcid.org/0000-0001-5297-9546 D
+ Author Affiliations
- Author Affiliations

A ECS Federal, in Support of National Marine Fisheries Service, Atlantic Highly Migratory Species Management Division, Silver Spring, MD, USA.

B National Marine Fisheries Service, Southeast Fisheries Science Center, Beaufort, NC, USA.

C The University of Southern Mississippi, Center for Fisheries Research and Development, Gulf Coast Research Laboratory, Ocean Springs, MS, USA.

D National Marine Fisheries Service, Southeast Fisheries Science Center, Pascagoula, MS, USA.

E Present address: Inter-American Tropical Tuna Commission, La Jolla, CA, USA.

* Correspondence to: dcrear8@gmail.com

Handling Editor: Colin Simpfendorfer

Marine and Freshwater Research 74(16) 1388-1403 https://doi.org/10.1071/MF23130
Submitted: 7 July 2023  Accepted: 5 October 2023  Published: 31 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Nursery areas provide refuge from predators, rich foraging grounds, and physical conditions conducive to growth and development of juvenile inhabitants. Specifically, the Mississippi Sound in the northern Gulf of Mexico is likely a nursery ground for multiple large and small coastal sharks.

Aims and methods

Using over a decade of shark survey catch data, we employed habitat modelling approaches to identify preferred environmental conditions and spatial distribution, and quantify core habitat overlap within the Mississippi Sound for young-of-year (YOY), juvenile and adult life stages of four coastal shark species.

Results

YOY Atlantic sharpnose (Rhizoprionodon terraenovae), blacktip (Carcharhinus limbatus) and finetooth (Carcharhinus isodon) sharks showed a preference for a combination of shallow, warm, low salinity, low dissolved oxygen and turbid waters. Corresponding to shared environmental preferences, spatial distributions of YOY sharks showed a high degree of overlap, particularly in the northern portion of the Mississippi Sound where few adult sharks were observed, suggesting that these life stages partition themselves to avoid predation.

Conclusion and implications

With a continued rise in US coastal shark populations, we hope this study can help further refine essential fish habitat for these coastal species and provide a framework analysis that can be used to understand habitat partitioning in other regions.

Keywords: coastal shark, delta-lognormal model, essential fish habitat, generalised additive mixed effects model, habitat model, life stages, nursey ground, predator avoidance, resource partitioning, species distribution model.

References

Aitchison J (1955) On the distribution of a positive random variable having a discrete probability mass at the origin. Journal of the American Statistical Association 50(271), 901-908.
| Crossref | Google Scholar |

Bangley CW, Paramore L, Shiffman DS, Rulifson RA (2018) Increased abundance and nursery habitat use of the bull shark (Carcharhinus leucas) in response to a changing environment in a warm-temperate estuary. Scientific Reports 8(1), 6018.
| Crossref | Google Scholar | PubMed |

Bangley CW, Curtis TH, Secor DH, Latour RJ, Ogburn MB (2020) Identifying important juvenile dusky shark habitat in the Northwest Atlantic ocean using acoustic telemetry and spatial modeling. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 12(5), 348-363.
| Crossref | Google Scholar |

Baremore IE, Passerotti MS (2013) Reproduction of the blacktip shark in the Gulf of Mexico. Marine and Coastal Fisheries 5(1), 127-138.
| Crossref | Google Scholar |

Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, 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.
| Crossref | Google Scholar |

Bethea DM, Buckel JA, Carlson JK (2004) Foraging ecology of the early life stages of four sympatric shark species. Marine Ecology Progress Series 268, 245-264.
| Crossref | Google Scholar |

Bethea DM, Ajemian MJ, Carlson JK, Hoffmayer ER, Imhoff JL, Grubbs RD, Peterson CT, Burgess GH (2015) Distribution and community structure of coastal sharks in the northeastern Gulf of Mexico. Environmental Biology of Fishes 98(5), 1233-1254.
| Crossref | Google Scholar |

Brodie SJ, Thorson JT, Carroll G, Hazen EL, Bograd S, Haltuch MA, Holsman KK, Kotwicki S, Samhouri JF, Willis-Norton E, et al. (2020) Trade-offs in covariate selection for species distribution models: a methodological comparison. Ecography 43, 11-24.
| Crossref | Google Scholar |

Chin A, Kyne PM, Walker TI, McAuley RB (2010) An integrated risk assessment for climate change: analysing the vulnerability of sharks and rays on Australia’s Great Barrier Reef. Global Change Biology 16(7), 1936-1953.
| Crossref | Google Scholar |

Cortés E (2008) Comparative life history and demography of pelagic sharks. In ‘Sharks of the open ocean: biology, fisheries and conservation’. (Eds MD Camhi, EK Pikitch, EA Babcock) pp. 309–322. (Blackwell Publishing Ltd)

Crear DP, Brill RW, Bushnell PG, Latour RJ, Schwieterman GD, Steffen RM, Weng KC (2019) The impacts of warming and hypoxia on the performance of an obligate ram ventilator. Conservation Physiology 7(1), coz026.
| Crossref | Google Scholar |

Crear DP, Latour RJ, Friedrichs MAM, St-Laurent P, Weng KC (2020) Sensitivity of a shark nursery habitat to a changing climate. Marine Ecology Progress Series 652, 123-136.
| Crossref | Google Scholar |

Crear DP, Curtis TH, Durkee SJ, Carlson JK (2021) Highly migratory species predictive spatial modeling (PRiSM): an analytical framework for assessing the performance of spatial fisheries management. Marine Biology 168(10), 148.
| Crossref | Google Scholar |

DeAngelis BM, McCandless CT, Kohler NE, Recksiek CW, Skomal GB (2008) First characterization of shark nursery habitat in the United States Virgin Islands: evidence of habitat partitioning by two shark species. Marine Ecology Progress Series 358, 257-271.
| Crossref | Google Scholar |

Dhellemmes F, Smukall MJ, Guttridge TL, Krause J, Hussey NE (2021) Predator abundance drives the association between exploratory personality and foraging habitat risk in a wild marine meso-predator. Functional Ecology 35(9), 1972-1984.
| Crossref | Google Scholar |

Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, et al. (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology 31(21), 4773-4787.e8.
| Crossref | Google Scholar | PubMed |

Duncan KM, Holland KN (2006) Habitat use, growth rates and dispersal patterns of juvenile scalloped hammerhead sharks Sphyrna lewini in a nursery habitat. Marine Ecology Progress Series 312, 211-221.
| Crossref | Google Scholar |

Efron B, Tibshirani RJ (1993) ‘An introduction to the bootstrap.’ (CRC Press: New York, NY, USA)

Froeschke J, Stunz GW, Wildhaber ML (2010) Environmental influences on the occurrence of coastal sharks in estuarine waters. Marine Ecology Progress Series 407, 279-292.
| Crossref | Google Scholar |

Gibson-Reinemer DK, Ickes BS, Chick JH (2017) Development and assessment of a new method for combining catch per unit effort data from different fish sampling gears: multigear mean standardization (MGMS). Canadian Journal of Fisheries and Aquatic Sciences 74(1), 8-14.
| Crossref | Google Scholar |

Grubbs RD (2010) Ontogenetic shifts in movements and habitat use. In ‘Sharks and their relatives II: biodiversity, adaptive physiology, and conservation’. (Eds JC Carrier, JA Musick, MR Heithaus) pp. 319–350. (CRC Press: Boca Raton, FL, USA)

Gunter G (1963) The fertile fisheries crescent. Journal of the Mississippi Academy of Science 9, 286-290.
| Google Scholar |

Guttridge TL, Gruber SH, Franks BR, Kessel ST, Gledhill KS, Uphill J, Krause J, Sims DW (2012) Deep danger: intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Marine Ecology Progress Series 445, 279-291.
| Crossref | Google Scholar |

Hamilton BR, Shipley ON, Grubbs RD (2022) Multi-channel feeding by migratory sharks in a fluvial-dominated estuary. Estuarine, Coastal and Shelf Science 275, 107977.
| Crossref | Google Scholar |

Hartog JR, Hobday AJ, Matear R, Feng M (2011) Habitat overlap between southern bluefin tuna and yellowfin tuna in the east coast longline fishery – implications for present and future spatial management. Deep-Sea Research – II. Topical Studies in Oceanography 58(5), 746-752.
| Crossref | Google Scholar |

Hastie TJ, Tibshirani RJ (1990) ‘Generalized additive models.’ (CRC Press)

Hazen EL, Jorgensen S, Rykaczewski RR, Bograd SJ, Foley DG, Jonsen ID, Shaffer SA, Dunne JP, Costa DP, Crowder LB, et al. (2013) Predicted habitat shifts of Pacific top predators in a changing climate. Nature Climate Change 3(3), 234-238.
| Crossref | Google Scholar |

Hazen EL, Scales KL, Maxwell SM, Briscoe DK, Welch H, Bograd SJ, Bailey H, Benson SR, Eguchi T, Dewar H, et al. (2018) A dynamic ocean management tool to reduce bycatch and support sustainable fisheries. Science Advances 4(5), eaar3001.
| Crossref | Google Scholar |

Heithaus MR (2007) Nursery areas as essential shark habitats: a theoretical perspective. In ‘Shark nursery grounds of the Gulf of Mexico and the East Coast waters of the United States, Proceedings of the 50th American Fisheries Society Symposium’, 19 August 2002, Baltimore, MD, USA. (Eds CT McCandless, NE Kohler, HL Pratt Jr) pp. 3–13. (American Fisheries Society: Bethesda, MD, USA) doi:10.47886/9781888569810.ch1

Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unraveling the ecological importance of elasmobranchs. In ‘Sharks and their relatives II’. (Eds JC Carrier, JA Musick, MR Heithaus) pp. 611–637. (CRC Press)

Heithaus MR, Vaudo JJ, Kreicker S, Layman CA, Krützen M, Burkholder DA, Gastrich K, Bessey C, Sarabia R, Cameron K, et al. (2013) Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Marine Ecology Progress Series 481, 225-237.
| Crossref | Google Scholar |

Hendon JM, Hoffmayer ER, Driggers WB, III (2013) First record of a nurse shark, Ginglymostoma cirratum, within the Mississippi sound. Gulf and Caribbean Research 25(1), 137-139.
| Crossref | Google Scholar |

Heupel MR, Hueter RE (2002) Importance of prey density in relation to the movement patterns of juvenile blacktip sharks (Carcharhinus limbatus) within a coastal nursery area. Marine and Freshwater Research 53(2), 543-550.
| Crossref | Google Scholar |

Heupel MR, Simpfendorfer CA (2011) Estuarine nursery areas provide a low-mortality environment for young bull sharks Carcharhinus leucas. Marine Ecology Progress Series 433, 237-244.
| Crossref | Google Scholar |

Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series 337, 287-297.
| Crossref | Google Scholar |

Heupel MR, Kanno S, Martins APB, Simpfendorfer CA (2019) Advances in understanding the roles and benefits of nursery areas for elasmobranch populations. Marine and Freshwater Research 70(7), 897-907.
| Crossref | Google Scholar |

Higgs JM, Hoffmayer ER, Sulikowski JA, Driggers WB, Stiller DA, Hendon JM (2020) Reproductive biology of the finetooth shark (Carcharhinus isodon) in the northern Gulf of Mexico, with evidence of both annual and biennial reproduction. Marine and Freshwater Research 72(5), 693-708.
| Crossref | Google Scholar |

Hoffmayer ER, Driggers WB, III, Jones LM, Hendon JM, Sulikowski JA (2013) Variability in the reproductive biology of the Atlantic sharpnose shark in the Gulf of Mexico. Marine and Coastal Fisheries 5(1), 139-151.
| Crossref | Google Scholar |

Hueter R, Tyminski J (2007) Species-specific distribution and habitat characteristics of shark nurseries in Gulf of Mexico waters off peninsular Florida and Texas. In ‘Shark nursery grounds of the Gulf of Mexico and the east coast waters of the United States, Proceedings of the 50th American Fisheries Society Symposium’, 19 August 2002, Baltimore, MD, USA. (Eds CT McCandless, NE Kohler, HL Pratt Jr) pp. 193–223. (American Fisheries Society: Bethesda, MD, USA) doi:10.47886/9781888569810.ch13

Kinney MJ, Hussey NE, Fisk AT, Tobin AJ, Simpfendorfer CA (2011) Communal or competitive? Stable isotope analysis provides evidence of resource partitioning within a communal shark nursery. Marine Ecology Progress Series 439, 263-276.
| Crossref | Google Scholar |

Kneebone J, Chisholm J, Skomal GB (2012) Seasonal residency, habitat use, and site fidelity of juvenile sand tiger sharks Carcharias taurus in a Massachusetts estuary. Marine Ecology Progress Series 471, 165-181.
| Crossref | Google Scholar |

Knip DM, Heupel MR, Simpfendorfer CA (2010) Sharks in nearshore environments: models, importance, and consequences. Marine Ecology Progress Series 402, 1-11.
| Crossref | Google Scholar |

Latour RJ, Gartland J, Peterson CD (2022) Ontogenetic niche structure and partitioning of immature sandbar sharks within the Chesapeake Bay nursery. Marine Biology 169(6), 76.
| Crossref | Google Scholar |

Lombardi-Carlson LA, Cortés E, Parsons GR, Manire CA (2003) Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico. Marine and Freshwater Research 54(7), 875–-883.
| Crossref | Google Scholar |

Lowe CG (2002) Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kāne’ohe Bay, Ō’ahu, HI. Journal of Experimental Marine Biology and Ecology 278(2), 141-156.
| Crossref | Google Scholar |

Lynch PD, Nye JA, Hare JA, Stock CA, Alexander MA, Scott JD, Curti KL, Drew K (2015) Projected ocean warming creates a conservation challenge for river herring populations. ICES Journal of Marine Science 72(2), 374-387.
| Crossref | Google Scholar |

Matich P, Heithaus MR (2015) Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia 178(2), 347-359.
| Crossref | Google Scholar | PubMed |

McCandless C, Pratt H, Kohler N, Merson, Recksiek C (2007) Distribution, localized abundance, movements, and migrations of juvenile sandbar sharks tagged in Delaware Bay. In ‘Shark nursery grounds of the Gulf of Mexico and the East Coast waters of the United States, Proceedings of the 50th American Fisheries Society Symposium’, 19 August 2002, Baltimore, MD, USA. (Eds CT McCandless, NE Kohler, HL Pratt Jr) p. 45. (American Fisheries Society: Bethesda, MD, USA). doi:10.47886/9781888569810.ch4

Norton SL, Wiley TR, Carlson JK, Frick AL, Poulakis GR, Simpfendorfer CA (2012) Designating critical habitat for juvenile endangered smalltooth sawfish in the United States. Marine and Coastal Fisheries 4(1), 473-480.
| Crossref | Google Scholar |

Oh BZL, Sequeira AMM, Meekan MG, Ruppert JLW, Meeuwig JJ (2017) Predicting occurrence of juvenile shark habitat to improve conservation planning. Conservation Biology 31(3), 635-645.
| Crossref | Google Scholar | PubMed |

Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham SV, Barreto R, Fernando D, Francis MP, et al. (2021) Half a century of global decline in oceanic sharks and rays. Nature 589(7843), 567-571.
| Crossref | Google Scholar | PubMed |

Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Marine Ecology Progress Series 320, 239-251.
| Crossref | Google Scholar |

Papastamatiou YP, Caselle JE, Friedlander AM, Lowe CG (2009) Distribution, size frequency, and sex ratios of blacktip reef sharks Carcharhinus melanopterus at palmyra atoll: a predator-dominated ecosystem. Journal of Fish Biology 75(3), 647-654.
| Crossref | Google Scholar | PubMed |

Parsons GR, Hoffmayer ER (2005) Seasonal changes in the distribution and relative abundance of the Atlantic sharpnose shark Rhizoprionodon terraenovae in the North Central Gulf of Mexico. Copeia 2005(4), 914-920.
| Crossref | Google Scholar |

Parsons GR, Hoffmayer ER (2007) Identification and characterization of shark nursery grounds along the Mississippi and Alabama Gulf Coasts. In ‘Shark nursery grounds of the Gulf of Mexico and the East Coast waters of the United States, Proceedings of the 50th American Fisheries Society Symposium’, 19 August 2002, Baltimore, MD, USA. (Eds CT McCandless, NE Kohler, HL Pratt Jr) pp. 301–316. (American Fisheries Society: Bethesda, MD, USA) doi:10.47886/9781888569810.ch19

Parsons GR, Hoffmayer ER, Hendon JM, Bet-Sayad WV (2008) A review of shark reproductive ecology: life history and evolutionary implications. In ‘Fish reproduction’. (MJ Rocha, A Arukwe, BG Kapoor) pp. 435–469. (Taylor and Francis)

Peterson CD, Parsons KT, Bethea DM, Driggers WB, III, Latour RJ (2017a) Community interactions and density dependence in the southeast United States coastal shark complex. Marine Ecology Progress Series 579, 81-96.
| Crossref | Google Scholar |

Peterson CD, Belcher CN, Bethea DM, Driggers WB, III, Frazier BS, Latour RJ (2017b) Preliminary recovery of coastal sharks in the south-east United States. Fish and Fisheries 18, 845-859.
| Crossref | Google Scholar |

Platell ME, Potter IC, Clarke KR (1998) Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Marine Biology 131(4), 719-734.
| Crossref | Google Scholar |

Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86(2), 501-509.
| Crossref | Google Scholar |

Rabalais NN, Turner RE (2019) Gulf of Mexico hypoxia: past, present, and future. Limnology and Oceanography Bulletin 28(4), 117-124.
| Crossref | Google Scholar |

Rabalais NN, Turner RE, Díaz RJ, Justić D (2009) Global change and eutrophication of coastal waters. ICES Journal of Marine Science 66(7), 1528-1537.
| Crossref | Google Scholar |

Searle SR, Speed FM, Milliken GA (1980) Population marginal means in the linear model: an alternative to least squares means. The American Statistician 34(4), 216-221.
| Crossref | Google Scholar |

Sibly RM, Kodric-Brown A, Luna SM, Brown JH (2018) The shark–tuna dichotomy: why tuna lay tiny eggs but sharks produce large offspring. Royal Society Open Science 5(8), 180453.
| Crossref | Google Scholar | PubMed |

Simpfendorfer CA, Milward NE (1993) Utilisation of a tropical bay as a nursery area by sharks of the families Carcharhinidae and Sphyrnidae. Environmental Biology of Fishes 37(4), 337-345.
| Crossref | Google Scholar |

Simpfendorfer CA, Freitas GG, Wiley TR, Heupel MR (2005) Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a Southwest Florida estuary. Estuaries 28(1), 78-85.
| Crossref | Google Scholar |

Stevens J, Bonfil R, Dulvy NK, Walker P (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57(3), 476-494.
| Crossref | Google Scholar |

Tickler DM, Letessier TB, Koldewey HJ, Meeuwig JJ (2017) Drivers of abundance and spatial distribution of reef-associated sharks in an isolated atoll reef system. PLoS ONE 12(5), e0177374.
| Crossref | Google Scholar | PubMed |

Turner RE, Rabalais NN, Justić D (2017) Trends in summer bottom-water temperatures on the northern Gulf of Mexico continental shelf from 1985 to 2015. PLoS ONE 12(9), e0184350.
| Crossref | Google Scholar | PubMed |

Ward-Paige CA, Britten GL, Bethea DM, Carlson JK (2015) Characterizing and predicting essential habitat features for juvenile coastal sharks. Marine Ecology 36(3), 419-431.
| Crossref | Google Scholar |

Wetherbee BM, Gruber SH, Rosa RS (2007) Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes. Marine Ecology Progress Series 343, 283-293.
| Crossref | Google Scholar |

White TD, Ferretti F, Kroodsma DA, Hazen EL, Carlisle AB, Scales KL, Bograd SJ, Block BA (2019) Predicted hotspots of overlap between highly migratory fishes and industrial fishing fleets in the northeast Pacific. Science Advances 5(3), eaau3761.
| Crossref | Google Scholar |

Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society Series B: Statistical Methodology 73(1), 3-36.
| Crossref | Google Scholar |

Wood SN (2017) ‘Generalized additive models: an introduction with R’, 2nd edn. (CRC Press: Boca Raton, FL, USA)

Yates PM, Heupel MR, Tobin AJ, Simpfendorfer CA (2015) Spatio-temporal occurrence patterns of young sharks in tropical coastal waters. Estuaries and Coasts 38(6), 2019-2030.
| Crossref | Google Scholar |