Trace metals pollution and trophic position of three sea urchin species in the Gulf of California.

Publisher: Kluwer Academic Publishers Country of Publication: United States NLM ID: 9885956 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-3017 (Electronic) Linking ISSN: 09639292 NLM ISO Abbreviation: Ecotoxicology Subsets: MEDLINE

Publication: 1999- : Boston : Kluwer Academic Publishers
Original Publication: London : Chapman & Hall,

Sea Urchins* ; Water Pollutants, Chemical*/analysis ; Environmental Monitoring*; Animals ; Metals, Heavy/analysis ; Food Chain ; Mexico

Sea urchin species are ecologically important in the Gulf of California and are becoming popular as a local fishery due to their commercial value. The most abundant species are Echinometra vanbrunti, Eucidaris thouarsii, and Tripneustes depressus. The objective of this study was to evaluate cadmium, lead, copper, zinc, and iron concentrations, as well as stable isotope values in these sea urchin species in the Santa Rosalia mining area (STR), in three sites: Punta Gorda, Punta el Aterrizaje, and Punta Salina. The highest Fe concentration (100.2 mg kg ^-1 ) was found in E. vanbrunti, while the highest concentrations of Pb (15.1 mg kg ^-1 ), Cu (14.5 mg kg ^-1 ), and Zn (347.7 mg kg ^-1 ) were recorded in E. thouarsii, and the highest Cd concentration (10.8 mg kg ^-1 ) was found in T. depressus. The main health risk of trace metal pollution in STR may be caused by Cd and Pb. δ ¹⁵ N and δ ¹³ C values were higher in E. thouarsii and T. depressus, respectively; E. thouarsii has the highest trophic position. Specimen size was not related to metal concentrations, but a positive relationship was observed between specimen size and isotopic values in T. depressus. The three species showed different bioaccumulation patterns for the metals analyzed. Additionally, collection sites and seasons play an important role in the variability of metal concentration.
(© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)

Ablanedo N, González H, Ramírez M, Torres I (1990) Evaluación del erizo de mar Echinometra lucunter como indicador de contaminación por metales pesados, Cuba. Aquat Living Resour 3:113–120. (PMID: 10.1051/alr:1990011)
Administration National Health Commission of PRC China Food and Drug Control (2018) The National Food Safety Standards-Food Contaminants set limit. Beijing, China.
Aquaculure Statistics F (2022) Global capture production 1950-2020. In: Fishery FAO, Aquatic statistics.
Archana A, Babu KR (2016) Nutrient composition and antioxidant activity of gonads of sea urchin Stomopneustes variolaris. Food Chem 197:597–602. (PMID: 10.1016/j.foodchem.2015.11.003)
Bautista-Romero J, Reyes-Bonilla H, Lluch-Cota D, Lluch-Cota S (1994) Aspectos generales de la fauna marina. In: Ortega-Rubio A, Catellanos-Vera A (eds) La Isla Socorro, Reserva de la Biósfera Archipiélago de Revillagigedo, 8th edn. Centro de Investigaciones Biologicas del Noreste, S.C., La Paz, Baja California Sur, Mexico, p 247–275.
Bohn A (1979) Trace metals in fucoid algae and purple sea urchins near a high Arctic lead/zinc ore deposit. Mar Pollut Bull 10:325–327. (PMID: 10.1016/0025-326X(79)90401-6)
Cadena-Cárdenas L, Méndez-Rodríguez L, Zenteno-Savín T et al. (2009) Heavy metal levels in marine mollusks from areas with, or without, mining activities along the Gulf of California, Mexico. Arch Environ Contam Toxicol 57:96–102. (PMID: 10.1007/s00244-008-9236-0)
Calva LG (2003) Hábitos alimenticios de algunos equinodermos. Parte 2 Erizos de mar y pepinos de mar. Contactos 47:54–63.
Cervantes C, Gutierrez-Corana F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137. (PMID: 10.1111/j.1574-6976.1994.tb00083.x)
Chen QX, Yang W, Chu QZ (2011) Assessments on contents of heavy metals in the edible parts of mollusks from Naozhou island, Zhanjiang. Ecol Environ Sci 20:175–180.
Chiarelli R, Martino C, Roccheri MC (2019) Cadmium stress effects indicating marine pollution in different species of sea urchin employed as environmental bioindicators. Cell Stress Chaperones 24:675–687. https://doi.org/10.1007/s12192-019-01010-1. (PMID: 10.1007/s12192-019-01010-1)
Colleta B, Angelier J (1981) Faulting evolution of the Santa Rosalia Basin, Baja California, Mexico. In: Proceedings of the Geology of Northwestern Mexico and Southern Arizona Congress. Universidad Nacional Autónoma de Mexico, Hermosillo, Sonora, Mexico, p 265–274.
Comisión N de A y (2016) Incrementó la producción de erizo de mar. Accessed 7 May 2024.
Conly AG, Scott SD, Bellon H (2011) Metalliferous manganese oxide mineralization associated with the Boléo Cu-Co Zn District, Mexico. Econ Geol 106:1173–1196. (PMID: 10.2113/econgeo.106.7.1173)
Cui Y, Chen BJ, Song YL (1997) Study on the content of heavy metals in marine organisms. J Appl Ecol 8:650–654.
Daesslé‚ LW, Ramos SE, Carriquiry JD, Camacho-Ibar VF (2002) Clay dispersal and the geochemistry of manganese in the Northern Gulf of California. Cont. Shelf Res 22:1311–1323. (PMID: 10.1016/S0278-4343(02)00007-9)
Farnham IM, Singh AK, Stetzenbach KJ, Johannesson KH (2002) Treatment of nondetects in multivariate analysis of groundwater geochemistry data. Chemom Intell Lab Syst 60:265–281. (PMID: 10.1016/S0169-7439(01)00201-5)
Flammang P, Warnau M, Temara A et al. (1997) Heavy metals in Diadema stosum (Echinodermata, Echinoidea) from Singapore coral reef. J Sea Res 38:35–45. (PMID: 10.1016/S1385-1101(97)00033-6)
Gao L, Huang X, Wang P et al. (2022) Concentrations and health risk assessment of 24 residual heavy metals in Chinese mitten crab (Eriocheir sinensis). Qual Assurance Saf Crops Foods 14:82–91. https://doi.org/10.15586/QAS.V14I1.1034. (PMID: 10.15586/QAS.V14I1.1034)
Gianguzza P, Badalamenti F, Giungazza F et al. (2009) The operational sex ratio of the sea urchin Paracantrotus lividus populations: the case of the Mediterranean marine protected area of Ustica Island (Tyrrhenian Sea, Italy). Mar Ecol 30:125–132. (PMID: 10.1111/j.1439-0485.2008.00267.x)
González-Peláez S (2004) Biología poblacional del erizo Echinometra vanbrunti (Echinodermata: Echinoidea), en el sur del golfo de California, México. Master thesis, Centro de investigaciones Biológicas del noroeste, SC.
Hamdoun A, Schrankel CS, Nesbit KT, Espinoza JA (2018) Sea urchin as lab animals for reproductive and developmental biology. Encyclopedia of reproduction. Second Edn.Elsevier, p 696–703. (PMID: 10.1016/B978-0-12-809633-8.20617-1)
Hernández OD, Gutiérrez ÁJ, González-Weller D et al. (2010) Accumulation of toxic metals (Pb and Cd) in the sea urchin Diadema aff. antillarum Philippi, 1845, in an Oceanic Island (Tenerife, Canary Islands). Environ Toxicol 25:227–233. https://doi.org/10.1002/tox.20487. (PMID: 10.1002/tox.20487)
Hernández-Almaraz P, Méndez-Rodríguez L, Zenteno-Savín T et al. (2016) Concentrations of trace elements in sea urchins and macroalgae commonly present in Sargassum beds: implications for trophic transfer. Ecol Res 31:785–798. https://doi.org/10.1007/s11284-016-1390-7. (PMID: 10.1007/s11284-016-1390-7)
Hernández-Almaraz P, Rivera MJ, Mazariegos-Villarreal A et al. (2022) Macroalgae contribution to the diet of two sea urchins in Sargassum Beds: Tripneustes depressus (Camarodonta: Toxopneustidae) and Eucidaris thouarsii (Cidaroide: Cidaridae). Reg Stud Mar Sci 53:102456. https://doi.org/10.1016/j.rsma.2022.102456. (PMID: 10.1016/j.rsma.2022.102456)
Holguín-Quiñones O, Wright López H, Solís Marín F (2000) Asteroidea, Echinoidea y Holothuroidea en fondos someros de la Bahía de Loreto, Baja California Sur, México. Rev Biol Trop 48:749–757.
Huerta-Diaz MA, Muñoz-Barbosa A, Otero XL et al. (2014) High variability in geochemical partitioning of iron, manganese and harmful trace metals in sediments of the mining port of Santa Rosalia, Baja California Sur, Mexico. J Geochem Explor 145:51–63. https://doi.org/10.1016/j.gexplo.2014.05.014. (PMID: 10.1016/j.gexplo.2014.05.014)
Hunting ER, Mulder C, Kraak MHS et al. (2013) Effects of copper on invertebrate-sediment interactions. Environ Pollut 180:131–135. (PMID: 10.1016/j.envpol.2013.05.027)
Jonathan MP, Shumilin E, Rodríguez-Figueroa GM et al. (2016) Potential toxicity of chemical elements in beach sediments near Santa Rosalía copper mine, Baja California Peninsula, Mexico. Estuar Coast Shelf Sci 180:91–96. https://doi.org/10.1016/j.ecss.2016.06.015. (PMID: 10.1016/j.ecss.2016.06.015)
Lawrence JM (2020) Sea urchins: biology and ecology, developments in aquaculture and fisheries science, Fourth ed. Academic Press.
Lawrence JM, Agatsuma Y (2013) Tripneustes. In: Lawrence JM (ed) Sea urchins: biology and ecology, Third Edit. Elsevier, p 491–597.
Martínez-Ayala JC, Galván-Magaña F, Tripp-Valdez A et al. (2022) Heavy metal concentrations in the Pacific sharpnose shark Rhizoprionodon longurio from the Santa Rosalia mining zone, Baja California Sur, Mexico. Mar Pollut Bull 182:114018. (PMID: 10.1016/j.marpolbul.2022.114018)
McCartney MA, Lessios HA (2002) Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol Bull 202:166–181. https://doi.org/10.2307/1543653. (PMID: 10.2307/1543653)
McClanahan TR, Muthiga N (2001) The ecology of Echinometra. In: Lawrence JM (ed) Edible Sea urchins: biology and ecology. Elsevier Science, New York, p 225–243.
Moureaux C, Simon J, Mannaerts G et al. (2011) Effects of the field contamination by metals (Cd, Cu, Pn, Zn) on biometry and mechanics of echinoderm ossicles. Aquat Toxiol 105:698–707. (PMID: 10.1016/j.aquatox.2011.09.007)
Nacci D, Serbst J, Gleason TR et al. (2000) Biological response of the sea urchin, Arbacia punctulata, lo lead contamination for an estuarine ecological risk assessment. J Aquat Ecosyst Stress Recov 7:187–199. (PMID: 10.1023/A:1009912609340)
Najjar TA, Tawaha MA, Wahsha M, Hilal AA (2018) Heavy metals in the sea urchin Diadema setosum from the Gulf of Aqaba. Fresenius Environ Bull 27:4149–4155.
Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750. (PMID: 10.1007/s002530051457)
Ohsumi Y, Kitamoto K, Anraku Y (1988) Change induced in the permeability barrier of the yeast plasma membrane by cupric ion. J Bacteriol 170:2676–2682. (PMID: 10.1128/jb.170.6.2676-2682.1988)
Olguín-Espinoza I (2000) La pesquería de erizo en México: Situación actual y perspectivas de desarrollo. Pesca Conserv 4:5–6.
Pérez-Tribouillier H, Shumilin E, Rodriguez-Figueroa GM (2015) Trace elements in the marine sediments of the La Paz Lagoon, Baja California Peninsula, Mexico: Pollution status in 2013. Bull Environ Contam Toxicol 95:61–66. (PMID: 10.1007/s00128-015-1520-x)
Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703–718. https://doi.org/10.2307/3071875. (PMID: 10.2307/3071875)
Post DM, Layman CA, Arrington DA et al. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x. (PMID: 10.1007/s00442-006-0630-x)
Quezada-Romegialli C, Jackson AL, Hayden B et al. (2018) TRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599. (PMID: 10.1111/2041-210X.13009)
R Core Team (2020) R: A language and environment for statistical computing. Vienna, Austria.
Reyes-Bonilla H (1995) Asteroidea and Echinoidea (Echinidermata) of Isla San Benedicto, Revillagigedo Archipielago, México. Rev Inv Ser Cient Ser Cienc Mar 6:29–38.
Reyes-Bonilla H, Calderón-Aguilera LE (1999) Population density, distribution and consumption rate of three corallivores at Cabo Pulmo reef, Gulf of California, México. Mar Ecol 20:347–357. (PMID: 10.1046/j.1439-0485.1999.2034080.x)
Rodríguez-Figueroa GM, Shumilin E, Sánchez-Rodríguez I (2009) Heavy metal pollution monitoring using the brown seaweed Padina durvillaei in the coastal zone of the Santa Rosalía mining region, Baja California Peninsula, Mexico. J Appl Phycol 21:10–26. (PMID: 10.1007/s10811-008-9346-0)
Rogers-Bennett L (2007) The ecology of Strongylocentrotus franciscanus and Strongylocentrotus purpuratus. Dev Aquacult Fish Sci 3:393–425.
Romero Gil JM (1991) El Boleo, Santa Rosalía, Baja California Sur: Un pueblo que se negó a morir, 1885–1954, UNISON-Gob. Sonora.
Salinas-Zavala CA, Lluch-Cota DB, Hernández-Vázquez S, Lluch-Belda D (1992) Anomalías de precipitación en Baja California Sur durante 1990. Posibles causas. Atmósfera 5:79–93.
Sánchez A, Shumilin E, Rodríguez-Figueroa G (2019) Sediment transport patterns inferred from grain size trends and trace metal dispersion near the Santa Rosalía mining district, Gulf of California. Sediment Geol 380:158–163. https://doi.org/10.1016/j.sedgeo.2018.12.006. (PMID: 10.1016/j.sedgeo.2018.12.006)
Sani RK, Peyton BM, Brown LT (2001) Copper-induced inhibition of growth of Desulfovibrio desulfuricans G20: assessment of its toxicity and correlation with those of Zinc and Lead. Appl Environ Microbiol 67:4765–4772. (PMID: 10.1128/AEM.67.10.4765-4772.2001)
Serviere-Zaragoza E, Lluch-Cota SE, Mazariegos-Villarreal A et al. (2021a) Cadmium, lead, copper, zinc, and iron concentration patterns in three marine fish species from two different mining sites inside the Gulf of California, Mexico. Int J Environ Res Public Health 18:1–18. https://doi.org/10.3390/ijerph18020844. (PMID: 10.3390/ijerph18020844)
Serviere-Zaragoza E, Mazariegos-Villarreal A, Balart EF et al. (2021b) Diet and trophic position of three common rocky reef fish at two locations in the Gulf of California. Reg Stud Mar Sci 47:101964. https://doi.org/10.1016/j.rsma.2021.101964. (PMID: 10.1016/j.rsma.2021.101964)
Shumilin E, Godinez-Orta L, Cruz Orozco R et al. (1996) Características litologo-geoquímicas de los sedimentos superficiales de Bahía Concepción,. BCS Actas INAGEQ 2:79–84.
Shumilin E, Jiménez-Illescas ÁR, López-López S (2013) Anthropogenic contamination of metals in sediments of the Santa Rosalía Harbor, Baja California Peninsula. Bull Environ Contam Toxicol 90:333–337. https://doi.org/10.1007/s00128-012-0923-1. (PMID: 10.1007/s00128-012-0923-1)
Shumilin E, Páez-Osuna F, Green-Ruiz C et al. (2001) Arsenic, antimony, selenium, and other trace elements in sediments of the La Paz Lagoon, Peninsula of Baja California, Mexico. Mar Pollut Bull 42:174–178. (PMID: 10.1016/S0025-326X(00)00123-5)
Shumilin EN, Rodriguez-Figueroa G, Morton Bermea O et al. (2000) Anomalous trace element composition of coastal sediments near the copper mining district of Santa Rosalia, Peninsula of Baja California, Mexico. Bull Environ Contam Toxicol 65:261–268.
Solís-Marín F, Honey-Escandón MB, Herrero-Perezrul MD, et al. (2013) The echinoderms of Mexico: biodiversity, distribution and current stage of knowledge. In: Alvarado JJ, Solís-Marín FA (eds) Echinoderm research and diversity in Latin America. Springer-Verlag Berlin Heidelberg, Berlin, pp 11–65.
Solís-Marín FA, Reyes-Bonilla H, Herrero-Pérezrul MD, Aripez-Covarrubias O (1997) Sistemática y distribución de los equinodermos de la Bahía de La Paz. Cienc Mar 23:249–263.
Søndergaard J, Hansson SV, Mosbech A, Bach L (2019) Green sea urchins (Strongylocentrotus droebachiensis) as potential biomonitors of metal pollution near a former lead-zinc mine in West Greenland. Environ Monit Assess 191. https://doi.org/10.1007/s10661-019-7637-3.
Soriano Bailón SE (2014) Evaluación de los bancos naturales del erizo negro (Echinometra vanbrunti) en la zona intermareal rocosa del balneario de Ballenita y comuna La Entrada, Provincia de Santa Elena, durante noviembre 2013-abril del 2014. Bachelor thesis, Universidad Estatla Península de Santa Elena, Ecuador.
Sonnenholzner-Varasa JI, Touronb N, Panchana Orralab MM (2018) Breeding, larval development, and growth of juveniles of the edible sea urchin Tripneustes depressus: A new target species for aquaculture in Ecuado. Aquac 496:134–145. (PMID: 10.1016/j.aquaculture.2018.07.019)
Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336. (PMID: 10.1016/0891-5849(94)00159-H)
Tellis MS, Lauer MM, Nadella S et al. (2014) Sublethal mechanisms of Pb and Zn toxicity to the purple sea urchin (Strongylocentrotus purpuratus) during early development. Aquat Toxicol 146:220–229. https://doi.org/10.1016/j.aquatox.2013.11.004. (PMID: 10.1016/j.aquatox.2013.11.004)
Templeton DM, Liu Y (2010) Multiple roles of cadmium in cell death and survival. Chem Biol Interact 188:267–275. (PMID: 10.1016/j.cbi.2010.03.040)
Thode-Andersen S, Jørgensen BB (1989) Sulfate reduction and the formation of 35S-labeled FeS2, and S0 in coastal marine sediments. Limnol Oceanogr 34:793–806. (PMID: 10.4319/lo.1989.34.5.0793)
Thorsen MS (1998) Microbial activity, oxygen status and fermentation in the gut of the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Mar Biol 132:423–433. https://doi.org/10.1007/s002270050408. (PMID: 10.1007/s002270050408)
Tigua H (2021) Caracterización de la Población del Erizo Negro en la Zona Intermareal Rocosa de Estero de Platano. Bachelor thesis, Pontificia Universidad Católica del Ecuador.
Toro-Farmer G, Cantera JR, Londono-Cruz E et al. (2004) Patrones de distribución y tasas de bioerosión del erizo Centrostephanus coronatus (Diadematoida: Diadematidae), en el arrecife de Playa Blanca, Pacífico colombiano. Rev Biol Trop 52:67–76. (PMID: 10.15517/rbt.v52i1.14703)
Vanderklify MA, Kendrick GA, Smit AJ (2006) Differences in trophic position among sympatric sea urchin species. Estuar Coast Shelf Sci 66:291–297. (PMID: 10.1016/j.ecss.2005.09.004)
Villalba Villalba AG, Chan Chan LH, Lagarda Diaz I et al. (2021) Reproductive cycle of sea urchin Echinometra vanbrunti (Echinodermata: Echinoidea) from the Gulf of California. Mar Biol Res 17:838–852. https://doi.org/10.1080/17451000.2022.2029901. (PMID: 10.1080/17451000.2022.2029901)
Vives A, Rubilar T, Herrero-Pérezrul MD, Ceballos-Vázquez BP (2021) Reproduction of the sea urchin Tripneustes depressus (Camarodonta: Toxopneustidae) in bahía de la paz, baja california sur, mexico. Rev Biol Trop 69:202–218. https://doi.org/10.15517/rbt.v69iSuppl.1.46353. (PMID: 10.15517/rbt.v69iSuppl.1.46353)
Warnau M, Ledent G, Temara A et al. (1995) Allometry of heavy metal bioconcentration in the echinoid Paracentrotus lividus (Echinodermata). Arch Environ Contam Toxicol 29:393–399. (PMID: 10.1007/BF00212506)
Wood SN (2017) Generalized additive models. An introduction with R, Second ed. Chapman & Hall.
Yesudas A, Vidyalakshmi D, Sivan G, Shameem K, Akhil Prakash E, Priyaja P (2023) Comparative analysis of temporal variation of heavy metal accumulation by two sea urchin species from a harbour region, including pre and post COVID 19 lock down period. Sci. Total Environ 877:162879.
Zhu G, Jin M, Song Wet al. (2015) Study on the harmful substances and food safety in the Ruditapes philippinarum at the Xiangshan Bay. In Proceedings of the international conference on chemical, material and food engineering 22:132–137. https://doi.org/10.2991/cmfe-15.2015.32.

CB2012 179327 Consejo Nacional de Ciencia y Tecnología

Keywords: Echinometra vanbrunti; Eucidaris thouarsii; Tripneustes depressus; Generalized additive models; Pollution index; Stable isotope

0 (Water Pollutants, Chemical)
0 (Metals, Heavy)

Date Created: 20240712 Date Completed: 20240828 Latest Revision: 20240828

20240828

10.1007/s10646-024-02778-4

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