Elsevier

Science of The Total Environment

Volumes 640–641, 1 November 2018, Pages 1500-1511
Science of The Total Environment

First record of bioaccumulation and bioconcentration of metals in Scleractinian corals and their algal symbionts from Kharg and Lark coral reefs (Persian Gulf, Iran)

https://doi.org/10.1016/j.scitotenv.2018.06.029Get rights and content

Highlights

  • The level of metals was assessed in corals and zooxanthellae from the Persian Gulf.

  • Differential metal bioaccumulation was found among Scleractinian coral species.

  • Metal accumulation was higher in coral tissues than skeletons.

  • Higher BCFs and BSAFs were found in zooxanthellae than coral tissues and skeletons.

  • Corals and zooxanthellae are useful bioindicators in coral reef monitoring.

Abstract

Metal pollution is nowadays a serious threat worldwide for ecosystem and human health. Despite that, there is still a paucity of data on metal impact on coral reef ecosystems. Herein, the levels of eleven metals (Mn, Zn, Cu, Cr, Co, Ni, V, As, Cd, Hg, Pb) were assessed in surface sediments, seawater samples, Scleractinian corals (tissue and skeleton) and their algal symbionts collected from Kharg and Lark coral reefs in the Persian Gulf, Iran. At Kharg, surface sediments and seawater showed higher concentrations of metals than Lark, attributable to the higher metal loads and petrochemical activities in the area. Sediment quality guidelines indicated Hg as a serious threat to biota both at Kharg and Lark. Accordingly, metals bioaccumulation and bioconcentration was higher in corals from Kharg relatively to Lark Island. Interestingly, as supported by values of BCFs and BSAFs, metal accumulation was higher in coral tissues in respect to skeletons, and in zooxanthellae relatively to coral tissues at both coral reefs. Differential metal bioaccumulation was found among Scleractinian species, indicating that corals have distinct selectivity for assimilating metals from ambient sediments and seawater. Overall, metal accumulation in corals and zooxanthellae is an appropriate tool for environmental monitoring studies in coral reefs. Noteworthy, the use of Porites lutea, among Scleractinian corals, seems to be as a good bioindicator in monitoring studies of metal pollution.

Introduction

Coral reefs, though usually considered as pristine environments, are worldwide affected by decreased biodiversity and a variety of stressors (Chan et al., 2014). The primary factors in provoking the deterioration of coral reefs are terrestrial and marine contamination (Brodie et al., 2012; Ranjbar Jafarabadi et al., 2017a, Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018; Tkachenko, 2017), as well as global warming and ocean acidification (Chan et al., 2012; Takesue et al., 2009; Tseng et al., 2011). Coral reef ecosystems are commonly impacted by anthropogenic changes in water quality, such as increased nutrient loads, augmented turbidity causing sedimentation and shading, and contamination by industrial compounds, metals and agro-chemicals (Brodie et al., 2012; Erftemeijer et al., 2012). In marine environments, toxic contaminants are potentially accumulated in sediments and biota, and subsequently transferred to humans through the food chain (Maisano et al., 2016; Pourang et al., 2005), provoking serious ecological and human health hazards. Among the innumerous inorganic and organic compounds discharged into marine environments, metals have received great attention because of their toxicity, persistence and potential to bioaccumulate in many species (Achary et al., 2017; Brandão et al., 2015; Cappello et al., 2016a, Cappello et al., 2016b, Cappello et al., 2017; De Domenico et al., 2013; Fasulo et al., 2012; Guerriero et al., 2002, Guerriero et al., 2003, Guerriero et al., 2014; Pejman et al., 2017; Ranjbar Jafarabadi et al., 2017c).

In aquatic monitoring, organisms like corals are considered as good bio-indicators of water quality (Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018). Determining metal accumulation in coral tissues and skeletons is useful to assess environmental changes and pollution (Al-Rousan et al., 2012; Esslemont, 2000; Mokhtar et al., 2012; Shen and Boyle, 1988), particularly in coral reefs increasingly impacted by anthropogenic factors. Elemental geochemistry has also been applied in coral skeletons to elucidate anthropogenic impacts of water quality within coral ecosystems (Chen et al., 2010). It is know that the discrepant mechanisms can incense the deposition of metals into corals (Mokhtar et al., 2012), therefore the growth of coral skeleton could modulate the metal assimilation between metal accumulation in skeleton and metal exposure in seawater. Hermatypic (or reef-building) corals are an endosymbiotic association between the Cnidarian host and photosynthetic algae, Symbiodinium spp. (Kuzminov et al., 2013). Zooxanthellae contribute over 95% of organic nutrients and carbon requirements of the host due to their photosynthetic activity, greatly enhancing the rates of calcification and development of a hard skeleton (Gattuso et al., 1999). Thus, any changes in photosynthesis rates due to environmental stressors could affect the coral symbiosis (Kuzminov et al., 2013; Ranjbar Jafarabadi et al., 2018).

Sediment quality inform about the anthropogenic input of trace elements in aquatic systems, because sediment act as a reservoir for metals due to their long residence time, and hence capacity of reflecting history of pollution in aquatic ecosystems (Tuna et al., 2007). As reported by Chan et al. (2012), the corals are able to absorb metals in their skeleton and tissues from aquatic environment, directly from seawater or through coral feeding. Hence, a careful evaluation of metals distribution in aquatic compartments should be necessary to plan a water management program. It is known that the coastlines of Kharg and Lark Islands, in the Persian Gulf (Iran) are exposed to high environmental risk from petrochemical contamination (Ranjbar Jafarabadi et al., 2017a, Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018). Kharg, for its crucial offshore position is a commercial harbor for crude oil export and loading, while Lark, adjacent to the Strait of Hormuz, is one of the Iranian major oil export points (Jupp et al., 2017; Ranjbar Jafarabadi et al., 2017a, Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018). Recently, due to the increasing pollution and environmental disasters in the region (including the world's biggest oil spill in 1991), concerns have been raised on the accelerating decline in water quality that could exceed the adaptive capacity of inshore coral communities, thus disrupting these ecosystems and their dependents.

Although metal accumulation in corals have been widely used to reveal the extent of metal pollution affecting reef environments worldwide (Chan et al., 2014; Chen et al., 2010; Esslemont, 2000; Mokhtar et al., 2012; Shen and Boyle, 1988), up to date only few studies assessed seawater and reef sediment pollution in Iranian Coral Islands (Ranjbar Jafarabadi et al., 2017a, Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018). Considering the urgency to adopt suitable environmental monitoring programs within the Persian Gulf, herein, it was accurately assessed, for the first time, the ecosystem health of Kharg and Lark coral reefs that have diverse coral species, which are handling with different pollution sources. Therefore, metal accumulation levels in several coral species (tissue and skeleton) and their symbionts were assessed in two regions of the Persian Gulf, together with sediment and water quality. The main objectives of this study were: (a) to determine the levels of As, Cd, Co, Cr, Cu, Hg, Mn, Ni, Pb, V, Zn in ambient sediments and seawater along with corals (skeleton, soft tissue and zooxanthellae), (b) to assess a possible relationship among the levels of metals in sediment, water and coral samples, (c) to evaluate a relationship between coral species and metal concentration, (d) to determine the bioaccumulation and bioconcentration of metals in coral skeleton, tissue and zooxanthellae, and (e) to assess the relationship between bioaccumulation and the present state of metals.

Section snippets

Study area

The Persian Gulf has a complex and unique tropical marine ecosystem, especially coral reefs, with relatively high biological diversity and many endemic species (Ranjbar Jafarabadi et al., 2018). Among the sixteen Islands within the Gulf, Kharg (29.235481°N 50.31°E) is a continental turtle-shell shaped Island at the north-west Persian Gulf and at 57 km north-west of Boushehr, one of the world's largest offshore crude oil terminal. Kharg is the main sea terminal for Iranian oil, equipped with

Sediment physical-chemical characterization and metal(loid)s contamination

Kharg sediment pore water pH varied from 6.57 to 9.95 with an overall mean of 6.88 (moderately acidic), while Lark sediment pore water pH ranged from 6.47 to 9.57 (mean of 7.93; moderately alkaline) (Table S2). Comparison among the sites at Kharg revealed that the station KH·ST2 showed a higher acidic pH than other sites (p < 0.05). No marked spatially variation trend of pH was found in Lark sediments, except for LA.ST2 (p < 0.05), in comparison to other Lark sites. The surface sediments of

Metal(loid)s availability in the Persian Gulf

Kharg reef has been subjected to a strong anthropogenic impact related to the intense petrochemical and petroleum activities (Ranjbar Jafarabadi et al., 2017a, Ranjbar Jafarabadi et al., 2017b, Ranjbar Jafarabadi et al., 2017c, Ranjbar Jafarabadi et al., 2018). In fact, the results reported herein pointed out higher levels of metal(loid)s in surface sediments and seawater from Kharg in relation to Lark. This is likely attributable to petroleum refinery discharging wastewaters containing a

Conclusion

The main conclusions of this study are the following:

  • -

    Metal accumulation in Scleractinian corals (skeleton, tissue and algal symbionts) of the Persian Gulf varied in accordance with environmental availability as indicated by metal levels in sediments and water. Therefore, the species selected here are good bioindicators of environmental contamination by metals.

  • -

    Bioaccumulation of metals in Persian corals is probably related with the impact of petrochemical activities in the area. According to

Capsule

Metals accumulation was assessed in Scleractinian corals (tissue and skeleton) and zooxanthellae, together with environmental compartments, from two coral reefs in the Persian Gulf, Iran.

Acknowledgement

This investigation was supported by the Academy of Environment Science of Tarbiat Modares University, in Tehran, Iran. We also would like to thank the Iranian Oil Terminal Company for facilitating the fieldwork.

References (65)

  • P.L. Erftemeijer et al.

    Environmental impacts of dredging and other sediment disturbances on corals: a review

    Mar. Pollut. Bull.

    (2012)
  • G. Esslemont

    Heavy metals in corals from Heron Island and Darwin harbour, Australia

    Mar. Pollut. Bull.

    (1999)
  • G. Esslemont

    Heavy metals in seawater, marine sediments and corals from the Townsville section, Great Barrier Reef Marine Park, Queensland

    Mar. Chem.

    (2000)
  • G. Guerriero et al.

    Stress-induced changes of plasma antioxidants in aquaculturred sea bass, Dicentrarchus labrax

    Comp. Biochem. Physiol. A Physiol.

    (2002)
  • D. Haynes et al.

    Organochlorine, heavy metal and polyaromatic hydrocarbon pollutant concentrations in the Great Barrier Reef (Australia) environment: a review

    Mar. Pollut. Bull.

    (2000)
  • B.P. Jupp et al.

    Assessment of heavy metal and petroleum hydrocarbon contamination in the Sultanate of Oman with emphasis on harbours, marinas, terminals and ports

    Mar. Pollut. Bull.

    (2017)
  • F. Kuzminov et al.

    Effects of metal toxicity on photosynthetic processes in coral symbionts, Symbiodinium spp

    J. Exp. Mar. Biol. Ecol.

    (2013)
  • X. Li et al.

    Heavy metal distribution in sediment profiles of the Pearl River estuary, South China

    Appl. Geochem.

    (2000)
  • M. Maisano et al.

    PCB and OCP accumulation and evidence of hepatic alteration in the Atlantic bluefin tuna, Thunnus thynnus, from the Mediterranean Sea

    Mar. Environ. Res.

    (2016)
  • M. Maisano et al.

    Effects of petrochemical contamination on caged marine mussels using a multi-biomarker approach: histological changes, neurotoxicity and hypoxic stress

    Mar. Environ. Res.

    (2017)
  • M.B. Mokhtar et al.

    Trace metal (Cd, Cu, Fe, Mn, Ni and Zn) accumulation in Scleractinian corals: a record for Sabah, Borneo

    Mar. Pollut. Bull.

    (2012)
  • S. de Mora et al.

    Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman

    Mar. Pollut. Bull.

    (2004)
  • H.A. Naser

    Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review

    Mar. Pollut. Bull.

    (2013)
  • A. Pejman et al.

    Fractionation of heavy metals in sediments and assessment of their availability risk: a case study in the northwestern of Persian Gulf

    Mar. Pollut. Bull.

    (2017)
  • S.-H. Peng et al.

    Bioaccumulation of trace metals in the submarine hydrothermal vent crab Xenograpsus testudinatus off Kueishan Island, Taiwan

    Mar. Pollut. Bull.

    (2011)
  • A. Ranjbar Jafarabadi et al.

    Spatial distribution and composition of aliphatic hydrocarbons, polycyclic aromatic hydrocarbons and hopanes in superficial sediments of the coral reefs of the Persian Gulf, Iran

    Environ. Pollut.

    (2017)
  • A. Ranjbar Jafarabadi et al.

    Comprehensive and comparative ecotoxicological and human risk assessment of polycyclic aromatichydrocarbons (PAHs) in reef surface sediments and coastal seawaters of Iranian Coral Islands, Persian Gulf

    Ecotoxicol. Environ. Saf.

    (2017)
  • A. Ranjbar Jafarabadi et al.

    Spatial distribution, ecological and health risk assessment of heavy metals in marine surface sediments and coastal seawaters of fringing coral reefs of the Persian Gulf, Iran

    Chemosphere

    (2017)
  • A. Ranjbar Jafarabadi et al.

    First report of bioaccumulation and bioconcentration of aliphatic hydrocarbons (AHs) and persistent organic pollutants (PAHs, PCBs and PCNs) and their effects on alcyonacea and scleractinian corals and their endosymbiotic algae from the Persian Gulf, Iran: inter and intra-species differences

    Sci. Total Environ.

    (2018)
  • A.J. Reichelt-Brushett et al.

    Trace metals in the living and nonliving components of scleractinian corals

    Mar. Pollut. Bull.

    (2003)
  • G.T. Shen et al.

    Determination of lead, cadmium and other trace metals in annually-banded corals

    Chem. Geol.

    (1988)
  • R.K. Takesue et al.

    Sources of land-derived runoff to a coral reef-fringed embayment identified using geochemical tracers in nearshore sediment traps

    Estuar. Coast. Shelf Sci.

    (2009)
  • Cited by (53)

    View all citing articles on Scopus
    View full text