Skip to main content
Log in

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

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

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. δ15N and δ13C 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.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

Data availability

The data that support this study will be shared upon reasonable request to the corresponding author.

References

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Calva LG (2003) Hábitos alimenticios de algunos equinodermos. Parte 2 Erizos de mar y pepinos de mar. Contactos 47:54–63

    Google Scholar 

  • Cervantes C, Gutierrez-Corana F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cui Y, Chen BJ, Song YL (1997) Study on the content of heavy metals in marine organisms. J Appl Ecol 8:650–654

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hunting ER, Mulder C, Kraak MHS et al. (2013) Effects of copper on invertebrate-sediment interactions. Environ Pollut 180:131–135

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Olguín-Espinoza I (2000) La pesquería de erizo en México: Situación actual y perspectivas de desarrollo. Pesca Conserv 4:5–6

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703–718. https://doi.org/10.2307/3071875

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rogers-Bennett L (2007) The ecology of Strongylocentrotus franciscanus and Strongylocentrotus purpuratus. Dev Aquacult Fish Sci 3:393–425

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Templeton DM, Liu Y (2010) Multiple roles of cadmium in cell death and survival. Chem Biol Interact 188:267–275

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vanderklify MA, Kendrick GA, Smit AJ (2006) Differences in trophic position among sympatric sea urchin species. Estuar Coast Shelf Sci 66:291–297

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

Download references

Acknowledgements

TAAP is a CONACYT postdoctoral fellow. We are grateful to Noemí Bocanegra Castillo, Horacio Bervera León, Jorge Angulo Calvillo, Enrique Calvillo Espinoza, Andrés González Peralta, Hugo A. Valencia Valdez (Centro de Investigaciones Biológicas del Noroeste, CIBNOR) and Alejandra Piño Gimate for technical support. To the Instituto Tecnológico de Mulegé for the facilities granted, and especially to M.C. Pablo Zambrano. María Elena Sánchez-Salazar edited the English manuscript. Finally, we want to thank the editor and the reviewers who provided insightful comments on this manuscript.

Funding

This work was supported by CIBNOR and Mexico’s Consejo Nacional de Ciencia y Tecnología [Grant #CB2012 179327].

Author information

Authors and Affiliations

Authors

Contributions

TAAP: Data generation, formal analysis, writing – original draft preparation. JMLV: Writing – review and editing. AMV: Methodology, data generation, writing – review and editing. LCMR: Writing – review and editing. KLC: Data generation, writing – review and editing. ROMR: Data analysis, writing – review and editing. ESZ: Conceptualization, data analysis, writing – review and editing, funding acquisition. All authors read and approved the manuscript.

Corresponding author

Correspondence to Elisa Serviere-Zaragoza.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

This work was conducted in compliance with all ethical standards. All necessary permits were obtained. Collection of wild samples of Tripneustes depressus, Echinometra vanbrunti, Eucidaris thouarsii were approved by Mexico’s Secretariat of Agriculture, Livestock, Rural Development, Fisheries, and Food (Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación) and CONAPESCA-México (#PPF/DGOPA-010/14).

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Acosta-Pachón, T.A., López-Vivas, J.M., Mazariegos-Villarreal, A. et al. Trace metals pollution and trophic position of three sea urchin species in the Gulf of California. Ecotoxicology 33, 786–800 (2024). https://doi.org/10.1007/s10646-024-02778-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-024-02778-4

Keywords

Navigation