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Marine Biodiversity

, Volume 49, Issue 2, pp 673–682 | Cite as

Species richness and spatial distribution of benthic amphipods (Crustacea: Peracarida) in the Alacranes Reef National Park, Gulf of Mexico

  • Carlos E. Paz-Ríos
  • Nuno Simões
  • Daniel PechEmail author
Original Paper
  • 208 Downloads

Abstract

The diversity and distribution of benthic amphipods has been explored in the Alacranes Reef, which is the largest coral reef ecosystem in the Gulf of Mexico. New insights into species richness, spatial distribution and extension of geographical ranges are presented by using data from published records and field surveys. A total of 117 species have been recorded, 9 of which are potentially new to science, 39 of which have new geographical records, and 7 are non-indigenous and previously reported in the literature as potentially invasive. Based on the use of a species-richness indicator (Chao 2), the expected species number is 40% higher, up to 200 spp., when compared to the observed species richness. The spatial distribution of amphipods varied significantly as a function of habitat type, showing the highest richness values on coral patches and the major abundances on man-made structures, such as navigation buoys and fishing traps. Multivariate analyses suggested the distinction between three taxonomically diverse species assemblages that showed similar ecological affinities, i.e. those on: (1) soft-bottom environments, grouping bare substrata and seagrass beds habitats; (2) hard-bottom environments, grouping coral patch and reef wall habitats; and (3) artificial substrata. The results highlight the importance of this reef ecosystem for a high amphipod diversity, but it is susceptible to future modifications in the presence of non-indigenous species, potentially invasive, on artificial substrata.

Keywords

Amphipoda Biodiversity Coral reefs Habitat heterogeneity Macroinfauna 

Notes

Acknowledgements

Thanks to Alfredo Gallardo, Fernando Mex (UNAM, Sisal) and the other expedition fellows for their help in the 2009 field work. A special thanks to the Oceanography Research Station of the Mexican Navy for the transportation and logistics assistance in Alacranes Reef. Diana Ugalde and Julio Duarte (UNAM, Sisal) helped with the thematic map. CONACYT provided a scholarship to C.P. We also thank two anonymous reviewers for their help in improving a previous version of the manuscript. The sampling permit number issued by the Mexican government (SAGARPA) was DGOPA/055592/120608.1481.

Compliance with ethical standards

Conflict of interest

The authors declare 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 by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Supplementary material

12526_2017_843_MOESM1_ESM.pdf (189 kb)
ESM 1 (PDF 188 kb)

References

  1. Acosta-González G, Arias-González JE (2010) Comunidades bentónicas del Arrecife Alacranes. In: Durán R, Méndez M (eds) Biodiversidad y Desarrollo Humano en Yucatán. CICY, Mérida, p 174Google Scholar
  2. Alarcón-Ortega L, Cupul-Magaña AL, Rodríguez-Troncoso AP, Cupul-Magaña FG (2017) Distribution and species richness of caprellids (Crustacea: Amphipoda) from the Mexican Pacific. Mar Biodivers Rec 10:9CrossRefGoogle Scholar
  3. Anderson MJ, Underwood AJ (1994) Effects of substratum on the recruitment and development of an intertidal estuarine fouling assemblage. J Exp Mar Biol Ecol 184:217–236CrossRefGoogle Scholar
  4. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525CrossRefGoogle Scholar
  5. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  6. Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202CrossRefGoogle Scholar
  7. Barnard JL (1970) Sublittoral Gammaridea (Amphipoda) of the Hawaiian islands. Smithson Contrib Zool 34:1–286CrossRefGoogle Scholar
  8. Bello-Pineda J, Liceaga-Correa MA, Hernández-Núñez H, Ponce-Hernández R (2005) Using aerial video to train the supervised classification of Landsat TM imagery for coral reef habitats mapping. Environ Monit Assess 105:145–164CrossRefGoogle Scholar
  9. Best RJ, Stachowicz JJ (2013) Phylogeny as a proxy for ecology in seagrass amphipods: which traits are most conserved? PLoS ONE 8:e57550CrossRefGoogle Scholar
  10. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VGW (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484CrossRefGoogle Scholar
  11. Carlton JT, Hodder J (1995) Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. Mar Biol 121:721–730CrossRefGoogle Scholar
  12. Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustac Biol 11:386–400CrossRefGoogle Scholar
  13. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  14. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  15. Clarke KR, Warwick RM (1998) A taxonomic distinctness index and its statistical properties. J Appl Ecol 35:523–531CrossRefGoogle Scholar
  16. Clarke KR, Warwick RM (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol Prog Ser 216:265–278CrossRefGoogle Scholar
  17. Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application published at: http://purl.oclc.org/estimates. Accessed 10 June 2015
  18. CONANP 2006 Programa de conservación y manejo. Parque Nacional Arrecife Alacranes. Mexico. CONANP, MéxicoGoogle Scholar
  19. Constable AJ (1999) Ecology of benthic macro-invertebrates in soft-sediment environments: a review of progress towards quantitative models and predictions. Austral Ecol 24:452–476CrossRefGoogle Scholar
  20. Cúrdia J, Carvalho S, Pereira F, Guerra-García JM, Santos MN, Cunha MR (2015) Diversity and abundance of invertebrate epifaunal assemblages associated with gorgonians are driven by colony attributes. Coral Reefs 34:611–624CrossRefGoogle Scholar
  21. Duarte J, Hermoso-Salazar M, Anker A, Simões N (2014) New records of alpheid shrimps (Crustacea: Decapoda: Alpheidae) from the southern Gulf of Mexico. Mar Biodivers Rec 7:e110CrossRefGoogle Scholar
  22. Ellingsen KE (2001) Biodiversity of a continental shelf soft-sediment macrobenthos community. Mar Ecol Prog Ser 218:1–15CrossRefGoogle Scholar
  23. Ellingsen KE, Clarke KR, Somerfield PJ, Warwick RM (2005) Taxonomic distinctness as a measure of diversity applied over a large scale: the benthos of the Norwegian continental shelf. J Anim Ecol 74:1069–1079CrossRefGoogle Scholar
  24. Ferreira CEL, Gonçalves JEA, Coutinho R (2006) Ship hulls and oil platforms as potential vectors to marine species introduction. J Coast Res Spec Issue 39:1340–1345Google Scholar
  25. Fisher R, O’Leary RA, Low-Choy S, Mengersen K, Knowlton N, Brainard RE, Caley MJ (2015) Species richness on coral reefs and the pursuit of convergent global estimates. Curr Biol 25:500–505CrossRefGoogle Scholar
  26. Gable MF, Lazo-Wasem EA, Baldinger AJ (2010) The Amphipoda of Bermuda-a century of taxonomy. Zool Beatica 21:131–141Google Scholar
  27. García-Madrigal MS (2007) Annotated checklist of the amphipods (Peracarida: Amphipoda) from the tropical eastern Pacific. In: Hendrickx ME (ed) Contributions to the study of East Pacific crustaceans 4(2). ICMyL-UNAM, México, pp 63–195Google Scholar
  28. García-Madrigal MS (2010) Littoral Maeridae and Melitidae (Amphipoda: Gammaridea) from the Gulf of Tehuantepec, Mexico. Zootaxa 2623:1–51CrossRefGoogle Scholar
  29. Glynn PW, Enochs IC (2011) Invertebrates and their roles in coral reef ecosystems. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, London, pp 273–325CrossRefGoogle Scholar
  30. Gotelli NJ, Chao A (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In: Levin SA (ed) Encyclopedia of biodiversity, 2nd edn. Academic, Waltham, pp 195–211CrossRefGoogle Scholar
  31. Guerra-Castro EJ, Cruz-Motta JJ (2014) Ecology of fouling assemblages associated with mangrove's roots: an artificial substrate for manipulative experiments. J Exp Mar Biol Ecol 457:31–40CrossRefGoogle Scholar
  32. Guerra-García JM (2003) Caprellids (Crustacea: Amphipoda) from Papua New Guinea, with the description of a new species. Helgol Mar Res 57:100–109CrossRefGoogle Scholar
  33. Hendrickx ME, Brusca RC, Ramírez-Reséndiz G (2002) Biodiversity of macrocrustaceans in the Gulf of California, Mexico. In: Hendrickx ME (ed) Contributions to the study of East Pacific crustaceans 1. ICMyL-UNAM, México, pp 349–368Google Scholar
  34. Hughes LE, Lowry JK (2010) Establishing a neotype for Elasmopus rapax Costa, 1853 and its presence as an invasive species in temperate Australian waters. J Crust Biol 30:699–709CrossRefGoogle Scholar
  35. Iannilli V, Vonk R (2013) A new Ingolfiellid (Crustacea, Amphipoda, Ingolfiellidae) from an anchialine pool on Abd al Kuri Island, Socotra archipelago, Yemen. ZooKeys 302:1–12CrossRefGoogle Scholar
  36. Jaume D, Iliffe TM, Van der Ham JL (2013) A new Psammogammarus (Amphipoda: Eriopisidae) from anchialine pools on the Exuma cays, Bahamas. Zootaxa 3700:48–64CrossRefGoogle Scholar
  37. Jebb MHP, Lowry JK (1995) Natural history of Madang lagoon with an appendix of collecting localities. In: Lowry JK (ed) the Amphipoda (Crustacea) of Madang lagoon, Papua New Guinea, part 1. Rec Austr Mus Suppl 22:1–24CrossRefGoogle Scholar
  38. Jordán-Dahlgren E, Rodríguez-Martínez RE (2003) The Atlantic coral reefs of Mexico. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 131–158CrossRefGoogle Scholar
  39. Kramer MJ, Bellwood DR, Bellwood O (2014) Benthic Crustacea on coral reefs: a quantitative survey. Mar Ecol Prog Ser 511:105–116CrossRefGoogle Scholar
  40. Krapp-Schickel T (2015) Minute but constant morphological differences within members of Stenothoidae: the Stenothoe gallensis group with four new members, keys to Stenothoe worldwide, a new species of Parametopa and Sudanea n. Gen. (Crustacea: Amphipoda). J Nat Hist 49:2309–2377CrossRefGoogle Scholar
  41. LeCroy SE (2002) An illustrated identification guide to the nearshore marine and estuarine gammaridean Amphipoda of Florida, volume 2, families Ampeliscidae, Amphilochidae, Amphithoidae, Aoridae, Argissidae and Haustoriidae. Florida Department of Environmental Protection, TallahasseeGoogle Scholar
  42. LeCroy SE (2011) An illustrated identification guide to the nearshore marine and estuarine gammaridean Amphipoda of Florida, volume 5, families Leucothoidae, Liljeborgiidae, Neomegamphopidae, Ochlesidae, Phliantidae, Phoxocephalidae, Platyischnopidae, Pleustidae, Podoceridae, Pontoporeiidae, Sebidae, Stenothoidae, Synopiidae and Talitridae. Florida Department of Environmental Protection, TallahasseeGoogle Scholar
  43. Liceaga-Correa MA, Hernández-Núñez H (2000) Localización y dimensiones del arrecife Alacranes. Jaina 11:8–10Google Scholar
  44. Liddell WD, Tunnell JW Jr (2011) Mexican reefs of the Gulf of Mexico. In: Buster NA, Holmes CW (eds) Gulf of Mexico – origin, waters, and biota, vol 3, Geology. Texas A&M University Press, Corpus Christi, pp 341–354Google Scholar
  45. Lowry JK (2006) The Amphipoda of New Caledonia. In: Payri CE, richer de forges B (eds) compendium of marine species of New Caledonia. Centre IRD, Nouméa, pp 239–245Google Scholar
  46. Lowry JK, Myers AA (2009) Benthic Amphipoda (Crustacea: Peracarida) of the great barrier reef. Zootaxa 2260:1–930Google Scholar
  47. Lowry JK, Myers AA (2017) A phylogeny and classification of the Amphipoda with the establishment of the new order Ingolfiellida (Crustacea: Peracarida). Zootaxa 4265:1–89CrossRefGoogle Scholar
  48. Martín A, Díaz Y, Miloslavich P, Escobar-Briones E, Guerra-García JM, Ortiz M, Valencia B, Giraldo A, Klein E (2013) Regional diversity of Amphipoda in the Caribbean Sea. Rev Biol Trop 61:1681–1720CrossRefGoogle Scholar
  49. Myers AA (1985) Shallow water coral reef and mangrove Amphipoda (Gammaridea) of Fiji. Rec Austr Mus 5:1–143CrossRefGoogle Scholar
  50. Myers AA (1997) Biogeographic barriers and the development of marine biodiversity. Estuar Coast Shelf Sci 44:241–248CrossRefGoogle Scholar
  51. Myers AA (2016) Amphipoda (Crustacea) from Palau, Micronesia: families Maeridae and Melitidae. Zootaxa 4170:451–474CrossRefGoogle Scholar
  52. Myers AA, Lowry JK (2009) The biogeography of indo-West Pacific tropical amphipods with particular reference to Australia. Zootaxa 2260:109–127Google Scholar
  53. Oliva-Rivera JJ (2003) The amphipod fauna of Banco Chinchorro, Quintana Roo, Mexico with ecological notes. Bull Mar Sci 73:77–89Google Scholar
  54. Ortegon-Aznar I, González-Vázquez DJ, Tuz-Sulub A, Aguilar-Perera A (2012) Cambio de fase alga-coral en el Parque Nacional Arrecife Alacranes, México: Una aproximación por grupos funcionales. Proceedings of the 65th Gulf and Caribbean Fisheries Institute, November 5–9, 2012 Santa Marta, Colombia, pp 136–139Google Scholar
  55. Ortigosa D, Lemus-Santana E, Simões N (2015) New records of ‘opisthobranchs’ (Gastropoda: Heterobranchia) from Arrecife Alacranes National Park, Yucatan, Mexico. Mar Biodivers Rec 8:e117CrossRefGoogle Scholar
  56. Ortiz M, Winfield I (2014) A new genus and species of Cyproideidae (Crustacea: Peracarida: Amphipoda) from a tropical coral reef, SE Gulf of Mexico. Zootaxa 3795:16–24CrossRefGoogle Scholar
  57. Paz-Ríos CE, Simões N, Ardisson P-L (2013a) Records and observations of amphipods (Amphipoda: Gammaridea and Corophiidea) from fouling assemblages in the Alacranes reef, southern Gulf of Mexico. Mar Biodivers Rec 6:e90CrossRefGoogle Scholar
  58. Paz-Ríos CE, Simões N, Ardisson P-L (2013b) Intertidal and shallow water amphipods (Amphipoda: Gammaridea and Corophiidea) from Isla Pérez, Alacranes reef, southern Gulf of Mexico. Nauplius 21:179–194CrossRefGoogle Scholar
  59. Paz-Ríos CE, Guerra-García JM, Ardisson P-L (2014) Caprellids (Crustacea: Amphipoda) from the Gulf of Mexico, with observations on Deutella mayeri, redescription of Metaprotella hummelincki, a taxonomic key and zoogeographical comments. J Nat Hist 48:2517–2578CrossRefGoogle Scholar
  60. Pech D, Ardisson P-L, Hernández-Guevara NA (2007) Benthic community response to habitat variation: a case of study from a natural protected area, the Celestun coastal lagoon. Cont Shelf Res 27:2523–2533CrossRefGoogle Scholar
  61. Plaisance L, Knowlton N, Paulay G, Meyer C (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28:977–986CrossRefGoogle Scholar
  62. Railkin AI (2005) Marine biofouling: colonization process and defenses. CRC, Boca RatonGoogle Scholar
  63. Rodríguez-Pliego P, Hernández-Arana HA, Ardisson P-L (2011) Partitioning spatial and temporal variability of tropical near-shore macrobenthic assemblages affected by natural and anthropogenic disturbances. Mar Freshw Res 62:342–349CrossRefGoogle Scholar
  64. Rumbold CE, Barlett TR, Gavio MA, Obenat SM (2016) Population dynamics of two invasive amphipods in the Southwestern Atlantic: Monocorophium acherusicum and Ericthonius punctatus (Crustacea). Mar Biol Res 12:268–277CrossRefGoogle Scholar
  65. Russ GR (1982) Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53:12–19CrossRefGoogle Scholar
  66. Stock JH, Vonk R (1992) Marine interstitial Amphipoda and isopoda (Crustacea) from Santiago, Cape Verde Islands. Bijdr Dierk 62:21–36Google Scholar
  67. Thomas JD (1993) Identification manual for the marine Amphipoda: (Gammaridea). I. Common coral reef and rock bottom amphipods of South Florida. Florida Department of Environmental Protection, TallahasseeGoogle Scholar
  68. Thomas JD, Klebba KN (2006) Studies of commensal leucothoid amphipods: two new sponge-inhabiting species from South Florida and the western Caribbean. J Crust Biol 26:13–22CrossRefGoogle Scholar
  69. Tolimieri N, Anderson MJ (2010) Taxonomic distinctness of demersal fishes of the California current: moving beyond simple measures of diversity for marine ecosystem-based management. PLoS ONE 5(5):e10653CrossRefGoogle Scholar
  70. Tunnell JW Jr, Chavez EA, Withers K (2007) Coral reefs of the southern Gulf of Mexico. Texas A&M University Press, Corpus ChristiGoogle Scholar
  71. Ugalde D, Gómez P, Simões N (2015) Marine sponges (Porifera: Demospongiae) from the Gulf of México, new records and redescription of Erylus trisphaerus (de Laubenfels, 1953). Zootaxa 3911:151–183CrossRefGoogle Scholar
  72. Underwood AJ, Chapman MG (2005) Design and analysis on benthic surveys. In: Eleftheriou A, McIntyre AD (eds) Methods for the study of marine benthos. Blackwell, Oxford, pp 1–42Google Scholar
  73. Vonk R, Gable M (2014) Infaunal zoogeography and intergeneric character blending: the case of Metaniphargus shiroi sp. nov. (Crustacea: Amphipoda: Hadziidae), from interstitial beach water on Akajima Island, the Kerama Islands, Southwestern Japan. Zool Sci 31:491–499CrossRefGoogle Scholar
  74. Vonk R, Jaume D (2014) Syntopy in rare marine interstitial crustaceans (Amphipoda, Ingolfiellidae) from small coral islands in the Molucca Sea, Incarried outsia. Mar Biodivers 44:163–172CrossRefGoogle Scholar
  75. White KN, Reimer JD (2012a) Commensal Leucothoidae (Crustacea, Amphipoda) of the Ryukyu archipelago, Japan. Part I: ascidian dwellers. ZooKeys 163:13–55CrossRefGoogle Scholar
  76. White KN, Reimer JD (2012b) Commensal Leucothoidae (Crustacea, Amphipoda) of the Ryukyu archipelago, Japan. Part II: sponge dwellers. ZooKeys 166:1–58CrossRefGoogle Scholar
  77. White KN, Reimer JD (2012c) Commensal Leucothoidae (Crustacea, Amphipoda) of the Ryukyu archipelago. Japan. Part III: coral rubble-dwellers. ZooKeys 173:11–50CrossRefGoogle Scholar
  78. Winfield I, Escobar-Briones E (2007) Anfípodos (Crustacea: Gammaridea) del sector norte del Mar Caribe: listado faunístico, registros nuevos y distribución espacial. Rev Mex Biodivers 78:51–61Google Scholar
  79. Winfield I, Ortiz M (2010) Colomastigids (Amphipoda: Gammaridea: Colomastigidae) from the Veracruz coral reef system, SW Gulf of Mexico, with a description of two new species associated with sponges. Sci Mar 74:773–782CrossRefGoogle Scholar
  80. Winfield I, Ortiz M (2012) A new species of Ensayara (Crustacea: Amphipoda: Endevouridae) from a tropical coral reef system, SW Gulf of Mexico. Bull Mar Sci 88:327–336CrossRefGoogle Scholar
  81. Winfield I, Ortiz M (2013a) The Caprellidea (Crustacea: Peracarida: Amphipoda) from the Gulf of Mexico with a description of a new species of Paracaprella. Sci Mar 77:161–168CrossRefGoogle Scholar
  82. Winfield I, Ortiz M (2013b) Curidia nunoi sp. nov. (Crustacea: Amphipoda: Ochlesidae), a new benthic species from a tropical coral reef southern Gulf of Mexico. J Mar Biol Assoc UK 94:353–359CrossRefGoogle Scholar
  83. Winfield I, Abarca-Arenas LG, Cházaro-Olvera S (2007) Crustacean macrofoulers in the Veracruz coral reef system, SW Gulf of Mexico: checklist, spatial distribution and diversity. Cah Biol Mar 48:287–295Google Scholar
  84. Winfield I, Cházaro-Olvera S, Ortiz M, Palomo-Aguayo U (2011) Lista actualizada de las especies de anfípodos (Peracarida: Gammaridea y Corophiidea) marinos invasores en México. Rev Biol Mar Oceanogr 46:349-361Google Scholar
  85. Winfield I, Muciño-Reyes MS, Ortiz M, Cházaro-Olvera S, Lozano-Aburto MA (2015) Biodiversidad de los anfípodos bentónicos (Peracarida: Amphipoda) asociados a macroalgas de Puerto Progreso, Yucatán, México. Rev Mex Biodivers 86:613–619CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratorio de Biodiversidad Marina y Cambio ClimaticoEl Colegio de la Frontera SurLermaMexico
  2. 2.Universidad Nacional Autonoma de Mexico, Facultad de CienciasUnidad Academica SisalSisalMexico
  3. 3.Laboratorio Nacional de Resiliencia Costera (LANRESC)SisalMexico
  4. 4.International Chair for Ocean and Coastal Studies, Harte Research InstituteTexas A&MCorpus ChristiUSA

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