Abstract
Intertidal and subtidal zones consist of heterogeneous habitats and dynamic environmental conditions, providing diverse options for fish to take advantage of marine resources. We explored how various environmental factors affected habitat use of an ecologically and economically important tropical marine fish, bonefish (Albula vulpes), on a fringing reef flat in Culebra, Puerto Rico, using a fine-scale acoustic telemetry positioning system. Machine learning algorithms and Bayesian inference via integrated nested Laplace approximation indicated diel period was the most important predictor of bonefish habitat use; bonefish occupied seagrass and mixed bottom (seagrass, macroalgae, sand) habitats most often at night, a deep-water soft sediment lagoon during the day, and infrequently used a shallow coral rubble reef crest. Zero-truncated (presence only) positioning frequency revealed more constrained utilization distributions during daytime and periods of higher water temperatures. Bonefish occupancy was highest in seagrass and mixed bottom habitats at lower water temperatures, and declined rapidly throughout the flat above 30 °C, which is consistent with temperature-mediated physiological constraints on performance (i.e. collapse of aerobic scope). Other factors including lunar phase, tidal state, and tide height had limited influence on bonefish habitat use. Building on a body of research, we propose several drivers of bonefish habitat use patterns amongst the diverse regions and habitats occupied, including predation risk, angling pressure, tidal variations, and temperature-related physiological performance. Our results emphasise the importance of conserving important seagrass foraging habitat through management and restoration.
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References
Adams AJ, Wolfe RK, Tringali MD, Wallace E, Kellison GT (2008) Rethinking the status of Albula spp. Biology in the Caribbean and western Atlantic. In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 203–216
Adams A, Guindon K, Horodysky A, MacDonald T, McBride R, Shenker J, Ward R (2012) The IUCN red list of threatened species 2012. IUCN. https://doi.org/10.2305/IUCN.UK.2012.RLTS.T194303A2310733.en
Allen AM, Singh NJ (2016) Linking movement ecology with wildlife management and conservation. Front Ecol Evol. https://doi.org/10.3389/fevo.2015.00155
Allgeier JE, Yeager LA, Layman CA (2013) Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems. Ecology 94:521–529. https://doi.org/10.1890/12-1122.1
Angilletta MJ (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509. https://doi.org/10.1093/icb/44.6.498
Ault JS (2008) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton
Barton PS, Lentini PE, Alacs E, Bau S, Buckley YM, Burns EL, Driscoll DA, Guja LK, Kujala H, Lahoz-Monfort JJ, Mortelliti A, Nathan R, Rowe R, Smith AL (2015) Guidelines for using movement science to inform biodiversity policy. Environ Manag 56:791–801. https://doi.org/10.1007/s00267-015-0570-5
Beguin J, Martino S, Rue H, Cumming SG (2012) Hierarchical analysis of spatially autocorrelated ecological data using integrated nested Laplace approximation. Methods Ecol Evol 3:921–929. https://doi.org/10.1111/j.2041-210X.2012.00211.x
Beitinger TL, Fitzpatrick LC (1979) Physiological and ecological correlates of preferred temperature in fish. Integr Comp Biol 19:319–329. https://doi.org/10.1093/icb/19.1.319
Breiman L (2001) Random forests. Mach Learn 45:5–32. https://doi.org/10.1023/A:1010933404324
Breiman L, Friedman J, Stone CJ, Olshen RA (1984) Classification and regression trees. Chapman & Hall/CRC, Boca Raton, FL
Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Board Can 21:1183–1226. https://doi.org/10.1139/f64-103
Brett JR (1969) Temperature and fish. Chesap Sci 10:275–276. https://doi.org/10.2307/1350466
Brownscombe JW, Gutowsky LFG, Danylchuk AJ, Cooke SJ (2014) Foraging behaviour and activity of a marine benthivorous fish estimated using tri-axial accelerometer biologgers. Mar Ecol Prog Ser 505:241–251. https://doi.org/10.3354/meps10786
Brownscombe JW, Cooke SJ, Algera DA, Hanson KC, Eliason EJ, Burnett NJ, Danylchuk AJ, Hinch SG, Farrell AP (2017a) Ecology of exercise in wild fish: integrating concepts of individual physiological capacity, behavior, and fitness through diverse case studies. Integr Comp Biol 139:437–449. https://doi.org/10.1093/icb/icx012
Brownscombe JW, Cooke SJ, Danylchuk AJ (2017b) Spatiotemporal drivers of energy expenditure in a coastal marine fish. Oecologia 183:689–699. https://doi.org/10.1007/s00442-016-3800-5
Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782. https://doi.org/10.1242/Jeb.084251
Cooke SJ, Martins EG, Struthers DP, Gutowsky LFG, Power M, Doka SE, Dettmers JM, Crook DA, Lucas MC, Holbrook CM, Krueger CC (2016) A moving target—incorporating knowledge of the spatial ecology of fish into the assessment and management of freshwater fish populations. Environ Monit Assess. https://doi.org/10.1007/s10661-016-5228-0
Crabtree R, Stevens C, Snodgrass D, Stengard F (1998) Feeding habits of bonefish, Albula vulpes, from the waters of the Florida Keys. Fish Bull 96:754–766
Crossin GT, Heupel MR, Holbrook CM, Hussey NE, Lowerre-Barbieri SK, Nguyen VM, Raby GD, Cooke SJ (2017) Acoustic telemetry and fisheries management. Ecol Appl 27:1031–1049. https://doi.org/10.1002/eap.1533
Cutler DR, Edwards TC, Beard KH, Cutler A, Hess KT, Gibson J, Lawler JJ (2007) Random forests for classification in ecology. Ecology 88:2783–2792. https://doi.org/10.1890/07-0539.1
Danylchuk AJ, Cooke SJ, Goldberg TL, Suski CD, Murchie KJ, Danylchuk SE, Shultz AD, Haak CR, Brooks EJ, Oronti A, Koppelman JB, Philipp DP (2011) Aggregations and offshore movements as indicators of spawning activity of bonefish (Albula vulpes) in The Bahamas. Mar Biol 158:1981–1999. https://doi.org/10.1007/s00227-011-1707-6
De’Ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192. https://doi.org/10.1890/0012-9658(2000)081%5b3178:CARTAP%5d2.0.CO;2
Diehl S (1992) Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73:1646–1661. https://doi.org/10.2307/1940017
Donaldson MR, Hinch SG, Suski CD, Fisk AT, Heupel MR, Cooke SJ (2014) Making connections in aquatic ecosystems with acoustic telemetry monitoring. Front Ecol Environ 12:565–573. https://doi.org/10.1890/130283
Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416. https://doi.org/10.1111/j.1461-0248.2004.00593.x
Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon population. Science (80-) 332:109–112
Espinoza M, Farrugia TJ, Webber DM, Smith F, Lowe CG (2011) Testing a new acoustic telemetry technique to quantify long-term, fine-scale movements of aquatic animals. Fish Res 108:364–371. https://doi.org/10.1016/j.fishres.2011.01.011
Finn JT, Brownscombe JW, Haak CR, Cooke SJ, Cormier R, Gagne T, Danylchuk AJ (2014) Applying network methods to acoustic telemetry data: modeling the movements of tropical marine fishes. Ecol Modell 293:139–149. https://doi.org/10.1016/j.ecolmodel.2013.12.014
Frezza PE, Clem SE (2015) Using local fishers knowledge to characterize historical trends in the Florida Bay bonefish population and fishery. Environ Biol Fishes 98:2187–2202. https://doi.org/10.1007/s10641-015-0442-0
Fry FEJ (1947) Effects of the environment on animal activity. Publ Ont Fish Res Lab 55:1–62. https://doi.org/10.1016/S1385-1101(99)00019-2
Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. https://doi.org/10.1126/science.1149345
Heck KL, Orth RJ (1980) Seagrass habitats: the roles of habitat complexity, competition and predation in structuring associated fish and motile macroinvertebrate assemblages. In: Kennedy VS (ed) Estuarine perspectives. Academic Press, Cambridge, Massachusetts, pp 449–464
Hothorn T, Zeileis A (2015) Partykit: a toolkit for recursive partytioning. J Mach Learn Res 16:3905–3909
Hothorn T, Hornik K, Zeileis A (2006) Unbiased recursive partitioning: a conditional inference framework. J Comput Graph Stat 15:651–674. https://doi.org/10.1198/106186006X133933
Hussey NE, Kessel ST, Aarestrup K, Cooke SJ, Cowley PD, Fisk AT, Harcourt RG, Holland KN, Iverson SJ, Kocik JF, Flemming JEM, Whoriskey FG (2015) Aquatic animal telemetry: a panoramic window into the underwater world. Science 348:1255642. https://doi.org/10.1126/science.1255642
Kessel ST, Cooke SJ, Heupel MR, Hussey NE, Simpfendorfer CA, Vagle S, Fisk AT (2014) A review of detection range testing in aquatic passive acoustic telemetry studies. Rev Fish Biol Fish 24:199–218
Kilgo JC, Labisky RF, Fritzen DE (1998) Influences of hunting on the behavior of white-tailed deer: implications for conservation of the Florida panther. Conserv Biol 12:1359–1364. https://doi.org/10.1111/j.1523-1739.1998.97223.x
Lapointe BE, Tomasko DA, Matzie WR (1994) Eutrophication and trophic state classification of seagrass communities in the Florida Keys. Bull Mar Sci 54:696–717
Larkin MF, Ault JS, Humston R, Luo J, Zurcher N (2008) Tagging of bonefish in south Florida to study population movements and stock dynamics. In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 301–322
Liaw A, Wiener M (2002) Classification and Regression by randomForest. R News 2:18–22. https://doi.org/10.1177/154405910408300516
Lima SL, Zollner PA (1996) Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol 11:131–135. https://doi.org/10.1016/0169-5347(96)81094-9
McLean MF, Simpfendorfer CA, Heupel MR, Dadswell MJ, Stokesbury MJW (2014) Diversity of behavioural patterns displayed by a summer feeding aggregation of Atlantic sturgeon in the intertidal region of Minas Basin, Bay of Fundy, Canada. Mar Ecol Prog Ser 496:59–69. https://doi.org/10.3354/meps10555
Meckley TD, Holbrook CM, Wagner C, Binder TR (2014) An approach for filtering hyperbolically positioned underwater acoustic telemetry data with position precision estimates. Anim Biotelemetry 2:7. https://doi.org/10.1186/2050-3385-2-7
Mitchell WA, Lima SL (2002) Predator-prey shell games: large-scale movement and its implications for decision-making by prey. Oikos 99:249–259. https://doi.org/10.1034/j.1600-0706.2002.990205.x
Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA, Merrill EH, Haydon DT (2010) Building the bridge between animal movement and population dynamics. Philos Trans R Soc B Biol Sci 365:2289–2301. https://doi.org/10.1098/rstb.2010.0082
Morris DW (2003) Toward an ecological synthesis: a case for habitat selection. Oecologia 136:1–13. https://doi.org/10.1007/s00442-003-1241-4
Murchie KJ, Cooke SJ, Danylchuk AJ, Suski CD (2011a) 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 Bio Ecol 396:147–155. https://doi.org/10.1016/j.jembe.2010.10.019
Murchie KJ, Cooke SJ, Danylchuk AJ, Danylchuk SE, Goldberg TL, Suski CD, Philipp DP (2011b) Thermal biology of bonefish (Albula vulpes) in Bahamian coastal waters and tidal creeks: an integrated laboratory and field study. J Therm Biol 36:38–48. https://doi.org/10.1016/j.jtherbio.2010.10.005
Murchie KJ, Cooke SJ, Danylchuk AJ, Danylchuk SE, Goldberg TL, Suski CD, Philipp DP (2013) Movement patterns of bonefish (Albula vulpes) in tidal creeks and coastal waters of Eleuthera, the Bahamas. Fish Res 147:404–412. https://doi.org/10.1016/j.fishres.2013.03.019
Murchie KJ, Shultz AD, Stein JA, Cooke SJ, Lewis J, Franklin J, Vincent G, Brooks EJ, Claussen JE, Philipp DP (2015) Defining adult bonefish (Albula vulpes) movement corridors around Grand Bahama in the Bahamian Archipelago. Environ Biol Fishes 98:2203–2212. https://doi.org/10.1007/s10641-015-0422-4
Murchie KJ, Haak CR, Power M, Shipley ON, Danylchuk AJ, Cooke SJ, Power M (2018) Ontogenetic patterns in resource use dynamics of bonefish (Albula vulpes) in the Bahamas. Environ Biol Fishes. https://doi.org/10.1007/s10641-018-0789-0
Naiman RJ (1988) How animals shape their ecosystems. Bioscience 38:750–752
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci 105:19052–19059. https://doi.org/10.1073/pnas.0800375105
Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217:244–251. https://doi.org/10.1242/jeb.089755
Nowell LB, Brownscombe JW, Gutowsky LFG, Murchie KJ, Suski CD, Danylchuk AJ, Shultz A, Cooke SJ (2015) Swimming energetics and thermal ecology of adult bonefish (Albula vulpes): a combined laboratory and field study in Eleuthera, The Bahamas. Environ Biol Fishes. https://doi.org/10.1007/s10641-015-0420-6
Orth RJ, Heck KL, van Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7:339–350
Özgül A, Lök A, Ulaş A, Düzbastilar FO, Tanrikul TT, Pelister C (2015) Preliminary study on the use of the Vemco Positioning System to determine fish movements in artificial reef areas: a case study on Sciaena umbra Linnaeus, 1758. J Appl Ichthyol 31:41–47. https://doi.org/10.1111/jai.12922
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science (80-) 315:95–97. https://doi.org/10.1126/science.1135471
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
RStudio Team (2016) RStudio: integrated development for R. RStudio Inc., Boston, MA. http://www.rstudio.com/
Roberts CM (1995) Effects of fishing on the ecosystem structure of coral reefs. Conserv Biol 9:988–995. https://doi.org/10.1046/j.1523-1739.1995.09050988.x
Rue H, Martino S, Chopin N (2009) Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J R Stat Soc Ser B Stat Methodol 71:319–392. https://doi.org/10.1111/j.1467-9868.2008.00700.x
Santos RO, Rehage JS, Adams AJ, Black BD, Osborne J, Kroloff EKN (2017) Quantitative assessment of a data-limited recreational bonefish fishery using a time-series of fishing guides reports. PLoS One 2:e0184776
Santos RO, Rehage JS, Kroloff EKN, Heinen JE, Adams AJ (2018) Combining data sources to elucidate spatial patterns in recreational catch and effort: fisheries-dependent data and local ecological knowledge applied to the South Florida bonefish fishery. Environ Biol Fishes. https://doi.org/10.1007/s10641-018-0828-x
Sargent FJ, Leary TJ, Crewz DW, Kruer CR (1995) Scarring of Florida’s seagrasses: assessment and management options. Florida Mar Res Inst Tech Reports 37
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480. https://doi.org/10.1016/S0169-5347(02)02580-6
Smith F (2013) Understanding HPE in the VEMCO Positioning System (VPS). Vemco 1–31. https://vemco.com/wp-content/uploads/2013/09/understanding-hpe-vps.pdf
Steel A, Coates J, Hearn A, Klimley A (2014) Performance of an ultrasonic telemetry positioning system under varied environmental conditions. Anim Biotelemetry 2:1–17. https://doi.org/10.1186/2050-3385-2-15
Stoner AW (1980) The role of seagrass biomass in the organization of benthic macrofaunal assemblages. Bull Mar Sci 30:537–551
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science (80-) 277:494–499. https://doi.org/10.1126/science.277.5325.494
Wickham H (2016) ggplot2: elegant graphics for data analysis. http://ggplot2.org. Accessed Aug 2017
Willette DA, Ambrose RF (2012) Effects of the invasive seagrass Halophila stipulacea on the native seagrass, Syringodium filiforme, and associated fish and epibiota communities in the Eastern Caribbean. Aquat Bot 103:74–82. https://doi.org/10.1016/j.aquabot.2012.06.007
Williams SL, Heck KLJ (2001) Seagrass community ecology. Mar Community Ecol. https://doi.org/10.2307/2679975
Williams JJ, Papastamatiou YP, Caselle JE, Bradley D, Jacoby DMP, Williams JJ (2018) Mobile marine predators : an understudied source of nutrients to coral reefs in an unfished atoll. Proc R Soc B. https://doi.org/10.1098/rspb.2017.2456
Zuur AF, Ieno EN, Saveliev AA (2017) Beginner’s guide to spatial, temporal, and spatial-temporal ecological data analysis with R-INLA. Highl Stat Ltd ISBN 978:1–12
Acknowledgements
We thank Dr. Craig Lilyestrom (Department of Natural and Environmental Resources, Commonwealth of Puerto Rico), Ricardo Colón-Merced, and Ana Roman (Culebra National Wildlife Refuges, US Fish and Wildlife Service), Capt. Chris Goldmark, Sammy Hernandez, Zorida Mendez, Henry Cruz, Sarah Becker, and Karl Anderson for their logistical support, and Temple Fork Outfitters, RIO Products, Costa Sunglasses, Patagonia Inc., Moldy Chum, and Umpqua Feather Merchants for their support. Thank you to the three reviewers and Editor, Dr. Ewan Hunter, for providing constructive feedback on this publication.
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Brownscombe is supported by a Banting Postdoctoral Fellowship and Bonefish and Tarpon Trust. This research was supported by the University of Puerto Rico Sea Grant Program awarded to A. J. Danylchuk, and J. Finn. Cooke was supported by NSERC and the Canada Research Chairs program. Additional funding for transmitters was provided by Brian Bennett, Brooks Patterson, Temple Fork Outfitters, and RIO Products. The authors have no conflicts of interest. All applicable international, national, and/or institutional guidelines for sampling, care, and experimental use of organisms for this study have been followed and all necessary approvals have been obtained. All procedures performed on bonefish were conducted in accordance with the Carleton University Animal Care Committee (application 11473), as well as the American Association for Laboratory Animal Science (IACUC protocol 2013-0031, University of Massachusetts Amherst). All research activities were conducted under a Puerto Rico Department of Natural Resources research permit #2-14-IC-034.
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Brownscombe, J.W., Griffin, L.P., Gagne, T.O. et al. Environmental drivers of habitat use by a marine fish on a heterogeneous and dynamic reef flat. Mar Biol 166, 18 (2019). https://doi.org/10.1007/s00227-018-3464-2
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DOI: https://doi.org/10.1007/s00227-018-3464-2