Abstract
We employed numerical wave models, GIS, and stable isotope analyses of otolith material to identify interspecific differences in habitat and resource use among juveniles of two sympatric and morphologically indistinct bonefishes, A. goreensis and A. vulpes in littoral zones of The Bahamas. Both species occurred in similar water temperatures; however, A. goreensis juveniles occupied habitats characterized by greater wave-driven flow velocities and closer proximity to coral reefs than A. vulpes. Likewise, A. goreensis was present across a broader range of flow environments and sampling stations than A. vulpes, which was typically confined to sheltered, low-flow habitats. The results of stable isotope analyses were consistent with the species’ relationships with environmental parameters, providing support for differential habitat and/or resource utilization. Otolith δ18O did not differ significantly between species, suggesting they experience comparable thermal regimes. However, δ13C varied substantially, with the otoliths of A. goreensis depleted in 13C relative to A. vulpes by approximately 1‰, potentially signifying a greater reliance on pelagic carbon sources by the former, in agreement with observed distinctions in habitat use. In linear models, otolith δ13C was negatively correlated with ambient flow velocity and positively related to distance from coral reef habitats, and these relationships did not vary across species. After accounting for the effects of these variables, species-specific differences in otolith δ13C remained, indicating that other unknown factors contributed to the observed disparities. Collectively, our findings suggest that niche partitioning between A. goreensis and A. vulpes is likely mediated by their differential abilities to compete across various flow environments, likely as a result of divergent behavioral and/or physiological adaptation.
Similar content being viewed by others
References
Adams AJ, Wolfe RK, Tringali MD, Wallace EM, Kellison GT (2007) Rethinking the status of Albula spp. biology in the Caribbean and western Atlantic. In: Ault J (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp p203–p215
Adams AJ, Horodysky AZ, McBride RS, Guindon K, Shenker J, MacDonald TC, Harwell HD, Ward R, Carpenter K (2014) Global conservation status and research needs for tarpons (Megalopidae), ladyfishes (Elopidae) and bonefishes (Albulidae). Fish Fish 15(2):280–311. https://doi.org/10.1111/faf.12017
Akin S, Buhan E, Winemiller KO, Yilmaz H (2005) Fish assemblage structure of Koycegiz lagoon–estuary, Turkey: spatial and temporal distribution patterns in relation to environmental variation. Estuar Coast Shelf Sci 64(4):671–684. https://doi.org/10.1016/j.ecss.2005.03.019
Anton A, Simpson MS, Vu I (2014) Environmental and biotic correlates to lionfish invasion success in Bahamian coral reefs. PLoS One 9(9):e106229. https://doi.org/10.1371/journal.pone.0106229
Arfi R, Guiral D, Bouvy M (1993) Wind induced resuspension in a shallow tropical lagoon. Estuar Coast Shelf Sci 36(6):587–604. https://doi.org/10.1006/ecss.1993.1036
Arlettaz R (1999) Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. J Anim Ecol 68(3):460–471. https://doi.org/10.1046/j.1365-2656.1999.00293.x
Bellwood D, Wainwright P (2001) Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the great barrier reef. Coral Reefs 20(2):139–150. https://doi.org/10.1007/s003380100156
Blaber SJM, Blaber TG (1980) Factors affecting the distribution of juvenile estuarine and inshore fish. J Fish Biol 17(2):143–162. https://doi.org/10.1111/j.1095-8649.1980.tb02749.x
Booij NR, Ris RC, Holthuijsen LH (1999) A third-generation wave model for coastal regions: 1. Model description and validation. J Geophys Res Oceans 104(C4):7649–7666. https://doi.org/10.1029/98JC02622
Boström C, O'Brien K, Roos C, Ekebom J (2006) Environmental variables explaining structural and functional diversity of seagrass macrofauna in an archipelago landscape. J Exp Mar Biol Ecol 335(1):52–73. https://doi.org/10.1016/j.jembe.2006.02.015
Bowen BW, Karl SA, Pfeiler E (2007) Resolving evolutionary lineages and taxonomy of bonefishes (Albula spp.). In: Ault J (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 147–153
Box GEP, Draper NR (1987) Empirical model-building and response surfaces. John Wiley & Sons
Brind'Amour A, Boisclair D, Legendre P, Borcard D (2005) Multiscale spatial distribution of a littoral fish community in relation to environmental variables. Limnol Oceanogr 50(2):465–479. https://doi.org/10.4319/lo.2005.50.2.0465
Bruger GE (1974) Age, growth, food habits, and reproduction of bonefish, Albula vulpes, in south Florida waters. Florida Marine Research Publications, No 3. Florida Department of Natural Resources, St Petersburg, FL
Buchan KC (2000) The Bahamas. Mar Pollut Bull 41(1):94–111. https://doi.org/10.1016/S0025-326X(00)00104-1
Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297
Clarke RD, Buskey EJ, Marsden KC (2005) Effects of water motion and prey behavior on zooplankton capture by two coral reef fishes. Mar Biol 146(6):1145–1155. https://doi.org/10.1007/s00227-004-1528-y
Clarke RD, Finelli CM, Buskey EJ (2009) Water flow controls distribution and feeding behavior of two co-occurring coral reef fishes: II. Laboratory experiments. Coral Reefs 28(2):475–488. https://doi.org/10.1007/s00338-009-0479-7
Colborn J, Crabtree RE, Shaklee JB, Pfeiler E, Bowen BW (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution 55(4):807–820. https://doi.org/10.1554/0014-3820(2001)055[0807:TEEOBA]2.0.CO;2
Cornelisen CD, Wing SR, Clark KL, Hamish BM, Frew RD, Hurd CL (2007) Patterns in the δ13C and δ15N signature of Ulva pertusa: interaction between physical gradients and nutrient source pools. Limnol Oceanogr 52(2):820–832. https://doi.org/10.4319/lo.2007.52.2.0820
Correia AT, Barros F, Sial AN (2011) Stock discrimination of European conger eel (Conger conger L.) using otolith stable isotope ratios. Fish Res 108(1):88–94. https://doi.org/10.1016/j.fishres.2010.12.002
Crabtree RE, Snodgrass DJ, Stengard FJ (2003) Bonefish species differentiation and delineation of critical juvenile habitat in the Florida Keys. In: Barbieri LR, Crabtree RE (eds) Five-year performance report to the US Department of Interior Fish and Wildlife Service from the Florida Fish and Wildlife Conservation Commission Florida Marine Research Institute, Investigations into nearshore and estuarine gamefish behavior, ecology, and life history in Florida. p 7–13
Crawley KR, Hyndes GA, Ayvazian SG (2006) Influence of different volumes and types of detached macrophytes on fish community structure in surf zones of sandy beaches. Mar Ecol Prog Ser 307:233–246
Crawley KR, Hyndes GA, Vanderklift MA, Revill AT, Nichols PD (2009) Allochthonous brown algae are the primary food source for consumers in a temperate, coastal environment. Mar Ecol Prog Ser 376:33–44. https://doi.org/10.3354/meps07810
Cummings M, J P (2001) Visual pigments and optical habitats of surfperch (Embiotocidae) in the California kelp forest. J Comp Physiol A 187(11):875–889. https://doi.org/10.1007/s00359-001-0258-6
Currey LM, Heupel MR, Simpfendorfer CA, Williams AJ (2014) Inferring movement patterns of a coral reef fish using oxygen and carbon isotopes in otolith carbonate. J Exp Mar Biol Ecol 456:18–25. https://doi.org/10.1016/j.jembe.2014.03.004
Cyrus D, Blaber S (1992) Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuar Coast Shelf Sci 35:545–563
Davis JP, Wing SR (2012) Niche partitioning in the Fiordland wrasse guild. Mar Ecol Prog Ser 446:207–220. https://doi.org/10.3354/meps09452
De la Morinière EC, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar Ecol Prog Ser 246:279–289
Deary AL, Metscher B, Brill RW, Hilton EJ (2016) Shifts of sensory modalities in early life history stage estuarine fishes (Sciaenidae) from the Chesapeake Bay using X-ray micro computed tomography. Environ Biol Fish 99(4):361–375. https://doi.org/10.1007/s10641-016-0479-8
Donovan MK, Friedlander AM, Harding KK, Schemmel EM, Filous A, Kamikawa K, Torkelson N (2015) Ecology and niche specialization of two bonefish species in Hawai‘i. Environ Biol Fish 98(11):2159–2171. https://doi.org/10.1007/s10641-015-0427-z
Dufour E, Gerdeaux D, Wurster CM (2007) Whitefish (Coregonus lavaretus) respiration rate governs intra-otolith variation of δ13C values in Lake Annecy. Can J Fish Aquat Sci 64(12):1736–1746. https://doi.org/10.1139/f07-132
Edmonds JS, Fletcher WJ (1997) Stock discrimination of pilchards Sardinops sagax by stable isotope ratio analysis of otolith carbonate. Mar Ecol Prog Ser 152(1/3):241–247
Elsdon TS, Ayvazian S, McMahon KW, Thorrold SR (2010) Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Mar Ecol Prog Ser 408:195–205. https://doi.org/10.3354/meps08518
Enders EC, Boisclair D, Roy AG (2003) The effect of turbulence on the cost of swimming for juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 60(9):1149–1160. https://doi.org/10.1139/f03-101
Fedler T (2010) The economic impact of flats fishing in the Bahamas. The Bahamian flats fishing alliance. Gainesville, Florida
Fedler T (2013) Economic impact of the Florida keys flats fishery. The bonefish and tarpon trust. Gainesville, Florida
Fenwick GD (1976) The effect of wave exposure on the amphipod fauna of the alga Caulerpa brownii. J Exp Mar Biol Ecol 25(1):1–18. https://doi.org/10.1016/0022-0981(76)90072-1
Finelli CM, Clarke RD, Robinson HE, Buskey EJ (2009) Water flow controls distribution and feeding behavior of two co-occurring coral reef fishes: I. Field measurements. Coral Reefs 28(2):461–473. https://doi.org/10.1007/s00338-009-0481-0
Finlay JC, Power ME, Cabana G (1999) Effects of water velocity on algal carbon isotope ratios: implications for river food web studies. Limnol Oceanogr 44(5):1198–1203. https://doi.org/10.4319/lo.1999.44.5.1198
Fonseca MS, Zieman JC, Thayer GW, Fisher JS (1983) The role of current velocity in structuring eelgrass (Zostera marina L.) meadows. Estuar Coast Shelf Sci 17(4):367–380. https://doi.org/10.1016/0272-7714(83)90123-3
Frezza PE, Clem SE (2015) Using local fishers’ knowledge to characterize historical trends in the Florida bay bonefish population and fishery. Environ Biol Fish 98(11):2187–2202. https://doi.org/10.1007/s10641-015-0442-0
Friedlander AM, Parrish JD (1998) Temporal dynamics of fish communities on an exposed shoreline in Hawaii. Environ Biol Fish 53(1):1–18. https://doi.org/10.1023/a:1007497210998
Fry B, Sherr EB δ13C Measurements as Indicators of Carbon Flow in Marine and Freshwater Ecosystems. In, New York, 1989. Stable Isotopes in Ecological Research. Springer New York, p 196–229
Fry B, Lutes R, Northam M, Parker PL, Ogden J (1982) A 13C/12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389–398. https://doi.org/10.1016/0304-3770(82)90112-7
Fulton CJ, Bellwood DR (2005) Wave-induced water motion and the functional implications for coral reef fish assemblages. Limnol Oceanogr 50(1):255–264. https://doi.org/10.4319/lo.2005.50.1.0255
Fulton CJ, Bellwood DR, Wainwright PC (2001) The relationship between swimming ability and habitat use in wrasses (Labridae). Mar Biol 139(1):25–33. https://doi.org/10.1007/s002270100565
Gabel F, Stoll S, Fischer P, Pusch MT, Garcia XF (2011) Waves affect predator-prey interactions between fish and benthic invertebrates. Oecologia 165(1):101–109. https://doi.org/10.1007/s00442-010-1841-8
Gao Y, Joner SH, Svec RA, Weinberg KL (2004) Stable isotopic comparison in otoliths of juvenile sablefish (Anoplopoma fimbria) from waters off the Washington and Oregon coast. Fish Res 68(1–3):351–360. https://doi.org/10.1016/j.fishres.2003.11.002
Godiksen JA, Svenning M-A, Dempson JB, Marttila M, Storm-Suke A, Power M (2010) Development of a species-specific fractionation equation for Arctic charr (Salvelinus alpinus (L.)): an experimental approach. Hydrobiologia 650(1):67–77. https://doi.org/10.1007/s10750-009-0056-7
Guiguer KRRA, Drimmie R, Power M (2003) Validating methods for measuring δ18O and δ13C in otoliths from freshwater fish. Rapid Commun Mass Spectrom 17(5):463–471. https://doi.org/10.1002/rcm.935
Haak CR, Cowles GW, Danylchuk AJ (2018) Wave and tide-driven flow act on multiple scales to shape the distribution of a juvenile fish (Albula vulpes) in shallow nearshore habitats. Limnol Oceanogr. https://doi.org/10.1002/lno.11063
Harborne AR et al (2008) Tropical coastal habitats as surrogates of fish community structure, grazing, and fisheries value. Ecol Appl 18(7):1689–1701. https://doi.org/10.1890/07-0454.1
Hartney KB (1989) The foraging ecology of two sympatric gobiid fishes: importance of behavior in prey type selection. Environ Biol Fish 26(2):105–118. https://doi.org/10.1007/bf00001027
Hidalgo M, Tomás J, Høie H, Morales-Nin B, Ninnemann US (2008) Environmental influences on the recruitment process inferred from otolith stable isotopes in Merluccius merluccius off the Balearic Islands. Aquat Biol 3:195–207. https://doi.org/10.3354/ab00081
Higgs ND, Newton J, Attrill MJ (2016) Caribbean spiny lobster fishery is underpinned by trophic subsidies from chemosynthetic primary production. Curr Biol 26(24):3393–3398. https://doi.org/10.1016/j.cub.2016.10.034
Hixon MA (1980) Competitive interactions between California reef fishes of the genus Embiotoca. Ecology 61(4):918–931. https://doi.org/10.2307/1936761
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120(3):314–326. https://doi.org/10.1007/s004420050865
Høie H, Folkvord A, Otterlei E (2003) Effect of somatic and otolith growth rate on stable isotopic composition of early juvenile cod (Gadus morhua L) otoliths. J Exp Mar Biol Ecol 289(1):41–58. https://doi.org/10.1016/s0022-0981(03)00034-0
Høie H, Otterlei E, Folkvord A (2004) Temperature-dependent fractionation of stable oxygen isotopes in otoliths of juvenile cod (Gadus morhua L.). ICES J Mar Sci 61(2):243–251. https://doi.org/10.1016/j.icesjms.2003.11.006
Holbrook SJ, Schmitt RJ (1989) Resource overlap, prey dynamics, and the strength of competition. Ecology 70(6):1943–1953. https://doi.org/10.2307/1938124
Hu X, Burdige DJ (2007) Enriched stable carbon isotopes in the pore waters of carbonate sediments dominated by seagrasses: evidence for coupled carbonate dissolution and reprecipitation. Geochim Cosmochim Acta 71(1):129–144. https://doi.org/10.1016/j.gca.2006.08.043
Hyndes GA, Platell ME, Potter IC (1997) Relationships between diet and body size, mouth morphology, habitat and movements of six sillaginid species in coastal waters: implications for resource partitioning. Mar Biol 128(4):585–598. https://doi.org/10.1007/s002270050125
Jamieson RE, Schwarcz HP, Brattey J (2004) Carbon isotopic records from the otoliths of Atlantic cod (Gadus morhua) from eastern Newfoundland, Canada. Fish Res 68(1–3):83–97. https://doi.org/10.1016/j.fishres.2004.02.009
Kalish JM (1991) 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Mar Ecol Prog Ser 75(2/3):191–203
Keddy PA (1982) Quantifying within-Lake gradients of wave energy: interrelationships of wave energy, substrate particle size and shoreline plants in axe lake, Ontario. Aquat Bot 14:41–58
Kieckbusch DK, Koch MS, Serafy JE, Anderson WT (2004) Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons. Bull Mar Sci 74(2):271–285
Lasiak T (1984) Structural aspects of the surf-zone fish assemblage at King's beach, Algoa Bay, South Africa: long-term fluctuations. Estuar Coast Shelf Sci 18(4):459–483
Lawson SE, Wiberg PL, McGlathery KJ, Fugate DC (2007) Wind-driven sediment suspension controls light availability in a shallow coastal lagoon. Estuar Coasts 30(1):102–112. https://doi.org/10.1007/bf02782971
Levin PS, Stunz GW (2005) Habitat triage for exploited fishes: can we identify essential “essential fish habitat?”. Estuar Coast Shelf Sci 64(1):70–78. https://doi.org/10.1016/j.ecss.2005.02.007
Lombarte A, Recasens L, Gonzalez M, de Sola LG (2000) Spatial segregation of two species of Mullidae (Mullus surmuletus and M. Barbatus) in relation to habitat. Mar Ecol Prog Ser 206:239–249
Lugendo BR, Nagelkerken I, van der Velde G, Mgaya YD (2006) The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. J Fish Biol 69(6):1639–1661. https://doi.org/10.1111/j.1095-8649.2006.01231.x
McMahon KW, Berumen ML, Mateo I, Elsdon TS, Thorrold SR (2011a) Carbon isotopes in otolith amino acids identify residency of juvenile snapper (family: Lutjanidae) in coastal nurseries. Coral Reefs 30(4):1135–1145. https://doi.org/10.1007/s00338-011-0816-5
McMahon KW, Fogel ML, Johnson BJ, Houghton LA, Thorrold SR, Gillanders B (2011b) A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids. Can J Fish Aquat Sci 68(8):1330–1340. https://doi.org/10.1139/f2011-070
McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol Oceanogr 58(2):697–714. https://doi.org/10.4319/lo.2013.58.2.0697
McMahon KW, Thorrold SR, Houghton LA, Berumen ML (2016) Tracing carbon flow through coral reef food webs using a compound-specific stable isotope approach. Oecologia 180(3):809–821. https://doi.org/10.1007/s00442-015-3475-3
McPherson ML, Zimmerman RC, Hill VJ (2015) Predicting carbon isotope discrimination in eelgrass (Zostera marinaL.) from the environmental parameters-light, flow, and [DIC]. Limnol Oceanogr 60(6):1875–1889. https://doi.org/10.1002/lno.10142
Minello TJ (1999) Nekton densities in shallow estuarine habitats of Texas and Louisiana and the identification of essential fish habitat in: Benaka L (ed) fish habitat: essential fish habitat and rehabilitation. American fisheries society. In: Symposium, vol 22. Bethesda, Maryland, pp 43–75
Nagelkerken I, van der Velde G (2004) Are Caribbean mangroves important feeding grounds for juvenile reef fish from adjacent seagrass beds? Mar Ecol Prog Ser 274:143–151
Nelson GA (2014) Cluster sampling: a pervasive, yet little recognized survey Design in Fisheries Research. Trans Am Fish Soc 143(4):926–938. https://doi.org/10.1080/00028487.2014.901252
Nelson J, Hanson CW, Koenig C, Chanton J (2011) Influence of diet on stable carbon isotope composition in otoliths of juvenile red drum Sciaenops ocellatus. Aquat Biol 13(1):89–95. https://doi.org/10.3354/ab00354
Pekcan-Hekim Z, Hellen N, Harkonen L, Nilsson PA, Nurminen L, Horppila J (2016) Bridge under troubled water: turbulence and niche partitioning in fish foraging. Ecol Evol 6(24):8919–8930. https://doi.org/10.1002/ece3.2593
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Pfeiler E (1996) Allozyme differences in Caribbean and gulf of California populations of bonefishes (Albula). Copeia 1996(1):181–183. https://doi.org/10.2307/1446953
Poff NL, Allan JD (1995) Functional organization of stream fish assemblages in relation to hydrological variability. Ecology 76(2):606–627
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Radtke RL, Lenz P, Showers W, Moksness E (1996) Environmental information stored in otoliths: insights from stable isotopes. Mar Biol 127(1):161–170. https://doi.org/10.1007/bf00993656
Rasmussen JB, Trudeau V (2010) How well are velocity effects on δ 13C signatures transmitted up the food web from algae to fish? Freshw Biol 55(6):1303–1314. https://doi.org/10.1111/j.1365-2427.2009.02354.x
Robertson AI, Lenanton RCJ (1984) Fish community structure and food chain dynamics in the surf-zone of sandy beaches: the role of detached macrophyte detritus. J Exp Mar Biol Ecol 84(3):265–283. https://doi.org/10.1016/0022-0981(84)90185-0
Roche DG, Taylor MK, Binning SA, Johansen JL, Domenici P, Steffensen JF (2014) Unsteady flow affects swimming energetics in a labriform fish (Cymatogaster aggregata). J Exp Biol 217(Pt 3):414–422. https://doi.org/10.1242/jeb.085811
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19(5):256–263. https://doi.org/10.1016/j.tree.2004.03.017
Santin S, Willis TJ (2007) Direct versus indirect effects of wave exposure as a structuring force on temperate cryptobenthic fish assemblages. Mar Biol 151(5):1683–1694. https://doi.org/10.1007/s00227-006-0586-8
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 12(9):e0184776. https://doi.org/10.1371/journal.pone.0184776
Sattler T, Bontadina F, Hirzel AH, Arlettaz R (2007) Ecological niche modelling of two cryptic bat species calls for a reassessment of their conservation status. J Appl Ecol 44(6):1188–1199. https://doi.org/10.1111/j.1365-2664.2007.01328.x
Schmitt RJ, Coyer JA (1982) The foraging ecology of sympatric marine fish in the genus Embiotoca (Embiotocidae): importance of foraging behavior in prey size selection. Oecologia 55(3):369–378. https://doi.org/10.1007/bf00376925
Schwalbe MAB, Webb JF (2014) Sensory basis for detection of benthic prey in two Lake Malawi cichlids. Zoology 117(2):112–121. https://doi.org/10.1016/j.zool.2013.09.003
Schwarcz HP, Gao Y, Campana S, Browne D, Knyf M, Brand U (1998) Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 55(8):1798–1806. https://doi.org/10.1139/f98-053
Seyoum S, Wallace EM, Tringali MD (2008) Permanent genetic resources: twelve polymorphic microsatellite markers for the bonefish, Albula vulpes and two congeners. Mol Ecol Resour 8(2):354–356. https://doi.org/10.1111/j.1471-8286.2007.01954.x
Snelgrove PVR, Butman CA (1994) Animal-sediment relationships revisited: cause versus effect. Oceanogr Mar Biol Annu Rev 32:111–177
Snodgrass D, Crabtree RE, Serafy JE (2008) Abundance, growth, and diet of young-of-the-year bonefish (Albula spp.) off the Florida keys, USA. Bull Mar Sci 82(2):185–193
Solomon CT, Weber PK, Cech JJ Jr, Ingram BL, Conrad ME, Machavaram MV, Pogodina AR, Franklin RL (2006) Experimental determination of the sources of otolith carbon and associated isotopic fractionation. Can J Fish Aquat Sci 63(1):79–89. https://doi.org/10.1139/f05-200
Storm-Suke A, Dempson JB, Reist JD, Power M (2007) A field-derived oxygen isotope fractionation equation for Salvelinus species. Rapid Commun Mass Spectrom 21(24):4109–4116. https://doi.org/10.1002/rcm.3320
Thorrold SR, Campana SE, Jones CM, Swart PK (1997) Factors determining δ13C and δ18O fractionation in aragonitic otoliths of marine fish. Geochim Cosmochim Acta 61(14):2909–2919. https://doi.org/10.1016/S0016-7037(97)00141-5
Tohse H, Mugiya Y (2008) Sources of otolith carbonate: experimental determination of carbon incorporation rates from water and metabolic CO2, and their diel variations. Aquat Biol 1:259–268. https://doi.org/10.3354/ab00029
Trudeau V, Rasmussen JB (2003) The effect of water velocity on stable carbon and nitrogen isotope signatures of periphyton. Limnol Oceanogr 48(6):2194–2199. https://doi.org/10.4319/lo.2003.48.6.2194
Tue NT, Quy TD, Nhuan MT, Dung LV, Thai ND (2017) Tracing carbon transfer and assimilation by invertebrates and fish across a tropical mangrove ecosystem using stable isotopes. Mar Ecol 38(5). https://doi.org/10.1111/maec.12460
UNEP-WCMC, WorldFish Centre, WRI, TNC (2010) Global distribution of warm-water coral reefs, compiled from multiple sources including the Millennium Coral Reef Mapping Project. Version 1.3. Includes contributions from IMaRS-USF and IRD (2005), IMaRS-USF (2005) And Spalding et al. (2001). UNEP World Conservation Monitoring Centre, Cambridge
Wallace EM (2014) Assessing biodiversity, evolution, and biogeography in bonefishes (Albuliformes): resolving relationships and aiding management. University of Minnesota, Dissertation
Wallace EM, Tringali MD (2010) Identification of a novel member in the family Albulidae (bonefishes). J Fish Biol 76(8):1972–1983. https://doi.org/10.1111/j.1095-8649.2010.02639.x
Wallace EM, Tringali MD (2016) Fishery composition and evidence of population structure and hybridization in the Atlantic bonefish species complex (Albula spp.). Mar Biol 163(6). https://doi.org/10.1007/s00227-016-2915-x
Acknowledgements
The authors wish to thank Lucas Griffin, Justin Lewis, and Brittany Sims for their assistance with field and laboratory work. Special thanks are due to Liz Wallace for her help with genetic species identifications. We are likewise grateful to Aaron Shultz, Karen Murchie, and David Philipp for their support. We also thank our reviewers, including Mike Allen and Derke Snodgrass, for input that improved this manuscript substantively. This research was funded by Bonefish & Tarpon Trust (BTT) and conducted under University of Massachusetts IACUC protocol #2010-0005. Danylchuk is a BTT Research Fellow and is also supported by the National Institute of Food & Agriculture, U.S. Department of Agriculture, the Massachusetts Agricultural Experiment Station and Department of Environmental Conservation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 19 kb)
Rights and permissions
About this article
Cite this article
Haak, C.R., Power, M., Cowles, G.W. et al. Hydrodynamic and isotopic niche differentiation between juveniles of two sympatric cryptic bonefishes, Albula vulpes and Albula goreensis. Environ Biol Fish 102, 129–145 (2019). https://doi.org/10.1007/s10641-018-0810-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-018-0810-7