Skip to main content

Advertisement

SpringerLink
Log in

High intraspecific genetic connectivity in the Indo-Pacific bonefishes: implications for conservation and management

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Bonefishes (Genus Albula) across the global tropics support premier destination catch and release fisheries. In parts of the Indo-Pacific harvest also occurs, often unregulated. Vital information on species ranges and stock structure is lacking for the Indo-Pacific bonefishes. Population declines, data deficiencies, and the absence of management plans result in conservation concerns. Research on bonefishes has also been hindered by taxonomic uncertainty stemming from morphological cryptics and inconsistent nomenclature. Genetic identification is necessary for some bonefishes, due to highly conserved morphology. This study explores verified species occurrences and genetic connectivity for six Indo-Pacific bonefishes. Samples were obtained from 210 bonefish from 16 locations across the Indian and Pacific Oceans. Genetic identification was determined through cytochrome b sequence analyses and population structure assessed with 17 microsatellite loci. Two bonefishes (A. glossodonta and A. oligolepis) are partially sympatric, suggesting multiple species may be supporting the fishery. Additional data are required to fully elucidate fishery composition at local scales and the geographic extent of species ranges. The IUCN Red List vulnerable A. glossodonta may experience increased fishing pressure due to its extensive Indo-Pacific range. Stock structure data support intraspecific genetic connectivity across broad spatial scales. Results suggested weak, non-geographic, genetic population structure in A. glossodonta, and panmixia in A. oligolepis and A. gilberti. The present study highlights the need for further research, and suggests conservation and management strategies for the Indo-Pac bonefishes may need both local and regional components to prevent further declines and localized collapse.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams AJ, Horodysky AZ, McBride RS, Guindon K, Shenker J, MacDonald TC, Harwell HD, Ward R, Carpenter K (2013) Global conservation status and research needs for tarpons (Megalopidae), ladyfishes (Elopidae) and bonefishes (Albulidae). Fish Fish 15:280–311

    Article  Google Scholar 

  • Ahmed NS, El-Deek MS, Emara HI (1994) Heavy metals in the muscle and bone of some fish species from the Red Sea. J KAU Mar Sci 7:25–31

    Google Scholar 

  • Al-Jufaili SM, Hermosa G, Al-Shuaily SS, Mujaini AA (2010) Oman fish biodiversity. J KAU Mar Sci 21:3–51

    Google Scholar 

  • Allen GR, Erdmann MV (2009) Reef fishes of the Bird’s Head Peninsula, West Papua, Indonesia. Checklist 5:587–628

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2000) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000. Université de Montpellier II, Montpellier

    Google Scholar 

  • Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migrationdirection among multiple sampling locations. Genet 185(1):313–326

  • Bloch ME, Schneider JG (1801) Systema Ichthyologiae iconibus cx illustratum. Post obitum auctoris opus inchoatum absolvit, correxit, interpolavit J.G. Schneider, Saxo Berolini. Berolini, Berlin

  • Bowen BW, Karl SA, Pfeiler E (2008) Resolving evolutionary lineages and taxonomy of bonefishes (Albula spp.). In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 147–154

    Google Scholar 

  • Bunce M, Rodwell LD, Gibb R, Mee L (2008) Shifting baselines in fishers’ perceptions of island reef fishery degradation. Ocean Coast Manag 51:285–302

    Article  Google Scholar 

  • 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 55:807–820

    Article  CAS  PubMed  Google Scholar 

  • Cooke SJ, Hogan ZS, Butcher PA, Stokesbury MJ, Raghavan R, Gallagher AJ, Hammerschlag N, Danylchuk AJ (2014) Angling for endangered fish: conservation problem or conservation action? Fish Fish

  • Dahlgren C, Shenker JM, Mojica R (2008) Ecology of bonefish during the transition from late larvae to early juveniles. In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 155–178

    Google Scholar 

  • Danylchuk AJ, Danylchuk SE, Cooke SJ, Goldberg TL, Koppelman J, Philipp DP (2008) Ecology and management of bonefish (Albula spp) in the Bahamian Archipelago. In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC Press, Boca Raton, pp 79–92

    Google Scholar 

  • Donovan MK, Williams ID, Friedlander AM, Longnecker K, Beets JP, Bowen BW, Franklin EC (2011) Catalog of coral reef fish life history specimens for the Hawaiian Islands. Pacific Islands Fisheries Science Center Report H-11-05 to NOAA

  • Donovan S, Pezold F, Chen Y, Lynch B (2012) Phylogeography of Anguilla marmorata (Teleostei: Anguilliformes) from the eastern Caroline Islands. Ichthyol Res 59(1):70–76

    Article  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A (2010) Geneious version 6.1. [computer program] Created by Biomatters. Available from http://www.geneious.com/. Accessed 3/18/2015

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure harvester: a website and programfor visualizing structure output and implementing the Evanno method. Cons Genet Res 4(2):359–361

  • Ekman S (1953) Zoogeography of the sea. Sidgwick & Jackson Ltd., London

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters ofindividuals using the software structure: a simulation study. Mol Ecol14:2611–2620

  • Fedler AJ, Hayes C (2008) Economic impacts of recreational fishing for bonefish, permit and tarpon in Belize for 2007. Report prepared for Turneffe Atoll Trust: http://www.turneffeatoll.org/tat-action-plan/economic-study. Accessed 3/18/2015

  • Forsskål P (1775) Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quae in itinere orientali observavit. Hauniae, Moller, p 164

    Google Scholar 

  • Fricke R, Kulbicki M, Wantiez L (2011) Checklist of the fishes of New Caledonia, and their distribution in the Southwest Pacific Ocean (Pisces). Stuttg Bietr Naturkunde A Neue Ser 4:341–463

    Google Scholar 

  • Friedlander AM, Caselle JE, Beets J, Lowe CG, Bowen BW, Ogawa TK, Kelley KM, Calitri T, Lange M, Anderson BS (2008) Biology and ecology of the recreational bonefish fishery at Palmyra Atoll National wildlife refuge with comparisons to other Pacific islands. In: Ault JS (ed) Biology and Management of the World Tarpon and Bonefish Fisheries. CRC Press, Boca Raton, pp 27–56

    Google Scholar 

  • Gagnaire PA, Minegishi Y, Zenboudji S, Valade P, Aoyama J, Berrebi P (2011) Within-population structure highlighted by differential introgression across semipermeable barriers to gene flow in Anguilla marmorata. Evolution 65:3413–3427

    Article  PubMed  Google Scholar 

  • Hidaka K, Iwatsuki Y, Randall JE (2008) A review of the Indo-Pacific bonefishes of the Albula argentea complex, with a description of a new species. Ichthyol Res 55:53–64

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) Clumpp: a cluster matching and permutationprogram for dealing with label switching and multimodality in analysis ofpopulation structure. Bioinform 23(14):1801–1806

  • Johannes RE, Yeeting B (2000) I-Kiribati knowledge and management of Tarawa’s lagoon resources. Atoll Res Bull 489:1–24

    Article  Google Scholar 

  • Kumara TP, Dalpathadu KR (2012) Provisional checklist of marine fish of Sri Lanka. Report to Department of Oceanography and Marine Geology, University of Ruhuna, Matara

  • Kwun HJ, Kim JK (2011) A new species of bonefish, Albula koreana (Albuliformes: Albulidae) from Korea and Taiwan. Zootaxa 2903:57–63

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for the comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lobel PS, Lobel LK (2004) Annotated checklist of fishes of Wake Atoll. Pac Sci 58:65–90

    Article  Google Scholar 

  • Lugendo BR (2007) Utilisation by fishes of shallw-water habitatas including mangorves and seagrass beds along the Tanzanian Coast. PhD Thesis, Radboud University, The Netherlands

  • Macpherson E, Richer de Forges B, Schnabel K, Samadi S, Boisselier MC, Garcia-Rubies A (2010) Biogeography of the deep-sea galatheid squat lobsters of the Pacific Ocean. Deep-Sea Res I Oceanogr Res Pap 57:228–238

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2011) The CIPRES science gateway: a community resource for phylogenetic analyses. In Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery (p. 41). ACM.

  • Minegishi Y, Aoyama J, Yoshizawa N, Tsukamoto K (2012) Lack of genetic heterogeneity in the Japanese eel based on a spatiotemporal sampling. Coast Mar Sci 35:269–276

    Google Scholar 

  • Mojica R, Shenker JM, Harnden CW, Wagner DE (1995) Recruitment of bonefish, Albula vulpes, around Lee Stocking Island, Bahamas. Fish Bull 93:666–674

    Google Scholar 

  • Ni I, Kwok K (1999) Marine fish fauna in Hong Kong waters. Zool Stud 38:130–152

    Google Scholar 

  • Pfeiler E (2008) Resurrection of the name Albula pacifica (Beebe, 1942) for the shafted bonefish (Albuliformes: Albulidae) from the eastern Pacific. Rev Biol Trop 56:839–844

    PubMed  Google Scholar 

  • Pfeiler E, Watts T, Pugh J, Van der Heiden AM (2008) Speciation and demographic history of the Cortez bonefish, Albula sp. A (Albuliformes: Albulidae), in the Gulf of California inferred from mitochondrial DNA. J Fish Biol 73:382–394

    Article  CAS  Google Scholar 

  • Pfeiler E, Van der Heiden AM, Ruboyianes RS, Watts T (2011) Albula gilberti, a new species of bonefish (Albuliformes: Albulidae) from the Eastern Pacific, and a description of adults of the parapatric A. esuncula. Zootaxa 3088:1–14

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rambaut A (2009) FigTree version 1.3. 1 [computer program]. Available from: http://tree.bio.ed.ac.uk/software/figtree/. Accessed 3/17/2015

  • Rambaut A, Drummond AJ (2007) Tracer v1.4 [computer program] Available from: http://beast.bio.ed.ac.uk/Tracer. Accessed 3/17/2015

  • Rambaut A, Drummond AJ (2010) TreeAnnotator v1.6 [computer program] Available from: http://beast.bio.ed.ac.uk/programs. Accessed 3/17/2015

  • Ram-Bidesi V (2011) An economic assessment of destructive fishing methods in Kiribati: a case study of te ororo fishing in Tarawa. School of marine studies. The University of the South Pacific, Suva

    Google Scholar 

  • Ram-Bidesi V, Petaia S (2010) Socio-economic assessment of fishing practices by North and South Tarawa fishers in Kiribati. Report submitted to Secretariat of the Pacific regional Environment Programme and Fisheries Division, Ministry of Marine Resources Development, Kiribati, 30 July 2010

  • Randall JE (1986) 106 new records of fishes from the Marshall Islands. Bull Mar Sci 38:170–252

    Google Scholar 

  • Randall JE, Lim KKP (2000) A checklist of the fishes of the South China Sea. Raffles Bull Zool 8:569–667

    Google Scholar 

  • Randall JE, Earle JL, Hayes T, Pittman C, Severns M, Smith RJF (1993) Eleven new records and validations of shore fishes from the Hawaiian Islands. Pac Sci 47:222–239

    Google Scholar 

  • Reece JS, Bowen BW, Smith DG, Larson A (2010) Molecular phylogenetics of moray eels (Muraenidae) demonstrates multiple origins of a shell-crushing jaw (Gymnomuraena, echidna) and multiple colonizations of the Atlantic Ocean. Mol Phylogenet Evol 57:829–835

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sato N, Asahida T, Terashima HT, Hurbungs MD, Ida H (2008) Species composition and dynamics of larval and juvenile fishes in the surf zone of Mauritius. Environ Biol Fish 81:229–238

    Article  Google Scholar 

  • Seeto J, Baldwin WJ (2010) A checklist of the fishes of Fiji and a bibliography of Fijian fish. Division of marine studies technical report 1/2010. The University of the South Pacific, Suva

    Google Scholar 

  • Seyoum S, Wallace EM, Tringali MD (2008) Twelve polymorphic microsatellite markers for the bonefish, Albula vulpes and two congeners. Mol Ecol Resour 8:354–356

    Article  CAS  PubMed  Google Scholar 

  • Shaklee JB (1984) Family albulidae. In: Fischer and Bianchi, (eds). FAO Species Identification Sheets for Fishery Purposes; Western Indian Ocean (fishing area 51). Rome, FAO. Vol 1

  • Shaklee JB, Tamaru CS (1981) Biochemical and morphological evolution of Hawaiian bonefishes (Albula). Syst Biol 30:125–146

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tenorio MC (2013) Updates to the checklist of fishes of the CNMI. Report submitted to the Division of fish and wildlife, Commonwealth of the Northern Mariana Islands, September 2013

  • Tirado-Sanchez N, Ruiz D, Chiriboga A, Banks S (2013) CDF checklist of Galapagos fish. In: Bungartz, Herrera, Jaramillo, Tirado, Jimenez-Uzcategui, Ruiz, Guezou, Ziemmeck (eds) Charles Darwin Foundation Galapagos Species Checklist 18 Sep 2013

  • Tsai Y-HE (2011) PhyloGeoViz: a web-based program that visualizes genetic data on maps. Mol Ecol Resour 11:557–561

    Article  PubMed  Google Scholar 

  • Vowles EJ, Amos W (2006) Quantifying ascertainment bias and species-specific length differences in human and chimpanzee microsatellites using genome sequences. Mol Biol Evol 23:598–607

    Article  CAS  PubMed  Google Scholar 

  • Wallace EM (2014) Assessing biodiversity, evolution, and biogeography in bonefishes (Albuliformes): resolving relationships and aiding management. Dissertation, University of Minnesota

  • Wallace EM, Tringali MD (2010) Identification of a novel member in the family Albulidae (bonefishes). J Fish Biol 76:1972–1983

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S, Miller MJ, Aoyama J, Tsukamoto K (2011) Analysis of vertebral counts of the tropical anguillids, Anguilla megastoma, A. obscura, and A. reinhardtii, in the western South Pacific in relation to their possible population structure and phylogeny. Environ Biol Fish 91:353–360

    Article  Google Scholar 

  • Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Article  Google Scholar 

  • Whitehead PJP (1986) The synonymy of Albula vulpes (Linnaeus, 1758)(Teleostei, Albulidae). Cybium 10:211–230

    Google Scholar 

Download references

Acknowledgments

Sincere thanks for the assistance of many colleagues and volunteer anglers, without whom this study would not have been possible. Thanks to M. Tringali and two anonymous reviewers for editorial suggestions and C. Anderson for GIS assistance. This work was supported in part by the University of Minnesota Supercomputing Institute. Study funding was provided by the James Ford Bell Museum of Natural History Dayton and Rothman funds and a Lerner-Gray grant from the American Museum of Natural History.

Compliance with ethical standards

ᅟ

Conflict of interest

The author declares that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Author information

Authors and Affiliations

  1. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 8th Ave. S.E., St. Petersburg, FL, 33701, USA

    Elizabeth M. Wallace

Authors
  1. Elizabeth M. Wallace
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth M. Wallace.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wallace, E.M. High intraspecific genetic connectivity in the Indo-Pacific bonefishes: implications for conservation and management. Environ Biol Fish 98, 2173–2186 (2015). https://doi.org/10.1007/s10641-015-0416-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-015-0416-2

Keywords

Search

Navigation