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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2022 Jan 20;46(2):421–428. doi: 10.1007/s12639-021-01462-2

Metal uptake in Psettodes erumei and Hysterothylacium spp. larvae in the Persian Gulf: Evaluation of larvae as bio-indicator

Bahareh Sedaghat 1, Seyed Mahmoud Sadjjadi 1, Gholamhossein Mohebbi 2, Mohammad Rayani 3,4,✉
PMCID: PMC9177921  PMID: 35692462

Abstract

This study aimed to compare the concentrations of heavy metals in Psettodes erumei as host fish and larvae of Hysterothylacium spp. as its parasite. Moreover, to evaluate the larvae as bio-indicators the uptake of heavy metals, the infected and non-infected fish were also compared. Fresh P. erumei species (n = 19) were randomly sampled during four months from Bushehr County, Iran. The digestive tract of each fish was examined for nematode parasites using a stereomicroscopy. The isolated nematodes were identified, and content of Fe, Cu, Zn, Co, Ni, Cr, As, Cd, Hg, and Pb were measured using ICP-OES. The metal concentrations were simultaneously analyzed for the muscles of infected fish and their parasites, as well as non-infected ones. Of the 19 P. erumei examined, 13 (68.4%) P. erumei were infected with Hysterothylacium spp. larvae. The parasites had significantly higher level of Fe, Cu, Zn, and Ni (with mean value of 7.59, 0.572, 1.223, and 4.623 mg/kg, respectively) than the muscles of the host fishes (with mean value of 3.29, 0.0010, 0.586, and 0.277 mg/kg, respectively) (p < 0.05). Infected hosts showed significantly lower amounts of As element in their muscles (0.050 mg/kg) than non-infected hosts (0.113 mg/kg) (p < 0.05). The findings emphasize the potential role of Hysterothylacium spp. larvae as bio-indicators for monitoring heavy metals pollution in marine ecosystems.

Keywords: Heavy metals, Persian Gulf, Bio-indication, Hysterothylacium spp., Psettodes erumei, Nematode

Introduction

Monitoring heavy metal concentrations in water, sediment, and aquatic fauna is critical for public health. The relationship between pollution and parasitism in marine organisms, as well as the potential role of parasites as water quality indicators, has been increased interest in recent decades (Sures 2004a; Dural et al. 2011; Sures et al. 2017). Heavy metals are soluble but not decomposable in aquatic ecosystems. They are stored at the bottom of the marine ecosystem, where aquatic living species absorb them and store them in their tissues (De et al. 2010; Lee et al. 2019). Heavy metals, which include essential elements including, iron (Fe), copper (Cu), and zinc (Zn), and cobalt (Co), non-essential (nontoxic) elements like chromium (Cr) and nickel (Ni), as well as non-essential (toxic) elements such as cadmium (Cd), arsenic (As), lead (Pb), and mercury (Hg), accumulate in the environment and tissues of marine animals. These elements have adverse effects on the aquatic ecosystem, and it can be a public health concern to animals and humans (Järup 2003; De et al. 2010; Chiarelli & Roccheri 2014; Gu et al. 2015).

Among the many parasites present in fish, intestinal helminthic parasites, which act as indicator species for identifying heavy metal contamination, are of particular relevance for parasite ecology (Sures & Reimann 2003; Malek et al. 2007; Morsy et al. 2012; Nachev et al. 2013; Amini et al. 2013; Hassan et al. 2016; Tongo et al. 2018; Al-Hasawi 2019; Hassanine et al. 2019). Acanthocephalans have proven to be the most successful parasites in accumulating heavy metals due to their morphology, metabolism/physiology, and host location (Sures 2003, 2004b; Vidal-Martinez et al. 2010; Mehana et al. 2020). Moreover, nematodes, a parasitic that infect a wide range of host species in aquatic ecosystems, can collect and eliminate heavy metals considerably from the host tissue. This suggests that parasites can be a useful bio-indicator for heavy metal pollution (Dural et al. 2011; Morsy et al. 2012; Abdel-Ghaffar et al. 2015; Hassan et al. 2016; Erasmus et al. 2020; Rewaida et al. 2020). The function of Anisakid nematodes of the genus Hysterothylacium as a bio-indicator of heavy metal contamination has been studied in Iran and elsewhere (Dural et al. 2010; Khaleghzadeh-Ahangar et al. 2011; Mazhar et al. 2014; Abdel-Ghaffar et al. 2015).

The Persian Gulf, being one of the world's most economically important locations, is exposed to different contaminants, including heavy metals, due to the massive operations, oil and gas exploration and extraction, as well as the discharge of industrial and agricultural wastewaters (Cunningham et al. 2019; Khatir et al. 2020). Due to its geographical and climatic characteristics, the Persian Gulf's northern coast contains sensitive ecosystems. Many companies, such as oil, gas, and petrochemicals, discharge pollutants such as trace elements into the waters in this section of the Persian Gulf (Bibak et al. 2021). Evaluation of Bioaccumulation of Heavy Metals in fish species in various Iranian aquatic Habitats by Sheikhzadeh and Hamidian (2021) found that fish obtained from the Persian Gulf had the highest levels of heavy metals. One of the most consumed fish among the Persian Gulf residents is Psettodes erumei (Bloch & Schneider, 1801), which belongs to the group of flatfishes commonly known as Indian halibut. P. erumei is locally called "Chollabi" or ‘Kafshak tiz dandan’ in Bushehr County (Nozar et al. 2015) and is available all year in Persian Gulf fish markets. Despite considerable studies on pollution in the Persian Gulf's marine environment, there is little information on the accumulation of heavy metals in aquatic species and their parasites in this region. Therefore, this study aimed to compare the concentration of heavy metals in P. erumei as host fish and larvae of Hysterothylacium spp. as its parasite. Also, heavy metals uptake in infected fish was compared with non-infected ones and evaluated whether the larvae could be used as bioindicators.

Materials and methods

Study area

This study was conducted in Bushehr County, also known as Bandar-e Bushehr, located in southwestern Iran, on a vast plain that runs along the Persian Gulf Coast (28.9234° N, 50.8203° E) (Fig. 1). Fishing is one of the main economic activities in this area, and fish, especially Indian halibut (Psettodes erumei), is considered as a high nutritive food source in the diet of the locals (Mukundan and James 1978).

Fig. 1.

Fig. 1

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Map of Iran, Bushehr county location in Bushehr province

Materials

All chemicals and solvents used for extraction and analysis of samples were obtained from Merck Germany and heavy metal standards from sigma chemical companies.

Sample collection and preparation

A total of nineteen fresh P. erumei specimens were randomly collected during four months of sampling from fishers of Bushehr County. The samples were brought to the Helminthology Laboratory of Shiraz University of Medical Sciences. This fish is easily identifiable based on having a thicker body than most other flatfishes, largemouth with solid teeth, and a brown-gray body-color (Assadi and Dehghani 1997). The fishes were dissected, and the digestive tract was separated and was divided into several parts in phosphate-buffer saline (PBS) and examined under a stereomicroscope. The nematodes were isolated from the intestine of the fishes and identified based on the valid keys (Moravec et al. 1997; Abdel-Ghaffar et al. 2015; Nozar et al. 2015). Only Hysterothylacium spp. larvae were found in the 13 contaminated fish, and no other helminthic species were detected. Also, 400 mg of the epaxial muscle in the dorsal side of each fish was separated, washed with distilled water, and kept at -20 °C until analysis (Fig. 2).

Fig. 2.

Fig. 2

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A: Whole digestive tract, B and C: Dissected digestive tract D: Isolated nematodes, E: Larva terminated with a mucron, F: Head of the larva

Instrumentation and metal analysis

The isolated helminths and fish muscles were weighed to the nearest 0.01 mg (wet weight) and then homogenized completely. Briefly, after drying at 65 °C for 6 h, the samples were spiked at 50 µg/kg by an internal standard, included Bi, In, Sc, Tb, and Y, from the Reagecon Company. For sample preparation, 3 ml of concentrated, ultra-pure nitric acid was added to each sample and then digested at 120 °C for 3 h. The solution was diluted to 15 ml with deionized water, and injected into the device for quantitative analysis of metals Fe, Cu, Zn, Co, Ni, Cr, As, Cd, Hg, and Pb. All measurements were made using an Agilent 7500 Series ICP-MS (Agilent Technologies, USA). The Argon grade-6 was used as a carrier gas. The operating conditions of the instrument were RF Power of 1550 W, RF Matching of 1.66 V, carrier gas rate of 0.95 L/min, make up gas rate of 0.15 L/min, nebulizer pump of 0.1 rps, Extract1 of -1 V, Extract 2 of -170 V, cell entrance of -30 V, QP focus of 5 V, and cell exit of -30 V. If the results were not within the linear calibration range, the samples were diluted with the deionized water.

Statistical analysis

Data analysis was performed using a Mann–Whitney U test to compare the biochemical analysis between infected and non-infected fishes and between fish hosts and their nematodes. The statistical analyses were performed using the SPSS software program version 16 (SPSS Inc., Chicago, IL, USA). The Graph Pad PRISM version 8 statistical package was used to draw graphs.

Result

Element concentration in the host-parasite system

Of the 19 P. erumei examined, 13 (68.4%) were infected with Hysterothylacium spp. larvae, while the other 6 (31.6%) were free from any intestinal helminth parasites.

Heavy metals in the tissue of infected P. erumei and Hysterothylacium spp. larvae

Table 1 and Fig. 3 show the mean concentrations of heavy metals in the muscle of infected P. erumei and Hysterothylacium spp. larvae isolated from them. Six elements, including Fe, Cu, Zn, Ni, Cr, and Hg, were detected in higher amounts in the parasites than those in their host muscles, although, As, Cd, and Pb were found in higher concentrations in their host muscles. Fe, Cu, Zn, and Ni concentrations in Hysterothylacium spp. larvae were significantly higher than those in P. erumei muscles (p 0.05). However, the As element concentrations in P. erumei muscles were considerably higher than that in Hysterothylacium spp. larvae (p < 0.05). The mean concentrations of heavy metals in Hysterothylacium spp. larvae were in the following order: in the non-essential (toxic) elements: Hg > Pb > As > Cd, in the non-essential (nontoxic) elements: Ni > Cr > , and in the essential element: Fe > Zn > Cu > Co. In addition, the non-essential (toxic) elements Hg > Pb > As > Cd, the non-essential (nontoxic) elements Cr > Ni, and the essential elements Fe > Zn > Cu = Co had the highest mean concentrations in the infected P. erumei muscles.

Table 1.

Mean concentration of heavy metals (mg/kg) in the Hysterothylacium spp. larvae and the infected P. erumei muscles

Group Fe* Cu* Zn* Co Ni* Cr As* Cd Hg Pb
Hysterothylacium spp. larvae Mean (mg/kg) 7.59 0.572 1.223 0.001 4.623 0.338 0.009 0.003 0.278 0.082
SD  ± 3.84  ± 1.399  ± 1.669  ± .0002  ± 5.105  ± 0.131  ± 0.011  ± 0.007  ± 0.553  ± 0.074
P. erumei muscles Mean (mg/kg) 3.29 0.001 0.586 0.001 0.277 0.297 0.050 0.005 0.188 0.126
SD  ± 1.62  ± 0.00  ± 0.856  ± 0.00  ± 0.298  ± 0.078  ± 0.051  ± 0.009  ± 0.423  ± 0.288
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SD: Standard deviation; *: Indicate p < 0.05

Fig. 3.

Fig. 3

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Mean concentration of heavy metal (mg/kg) in the Hysterothylacium spp. larvae and the infected P. erumei muscles

Heavy metals in the tissue of infected and non-infected P. erumei

The mean concentrations of heavy metals in the tissue of infected and non-infected fishes are embedded in Table 2 and Fig. 4. Infected fish with parasites had lower Fe, Zn, As, and Hg concentrations than non-infected fish, while non-infected hosts had lower Ni, Cd, and Pb concentrations. Moreover, statistical analysis showed that the concentration of As element level in muscle of infected hosts was significantly lower than in muscle of non-infected hosts (p < 0.05). The mean concentrations of heavy metals in the non-infected P. erumei muscles were in the following order: in the non-essential (toxic) elements: Hg > As > Pb > Cd, in the non-essential (nontoxic) elements: Cr > Ni, and in the essential elements: Fe > Zn > Cu = Co.

Table 2.

Mean concentration of heavy metals (mg/kg) in the muscles of infected P. erumei with Hysterothylacium spp. larvae and non-infected fish

Fish Fe Cu Zn Co Ni Cr As* Cd Hg Pb
Infected Mean (mg/kg) 3.29 0.001 0.586 0.001 0.277 0.297 0.050 0.005 0.188 0.126
SD  ± 1.62  ± 0.00  ± 0.856  ± 0.00  ± 0.298  ± 0.078  ± 0.051  ± 0.009  ± 0.423  ± 0.288
Non-infected Mean (mg/kg) 3.417 0.001 1.201 0.001 0.105 0.278 0.113 0.001 0.947 0.055
SD  ± 1.3.8  ± 0.00  ± 2.151  ± 0.00  ± 0.062  ± 0.138  ± 0.078  ± 0.009  ± 1.904  ± 0.044
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SD: Standard deviation; *: Indicate p < 0.05

Fig. 4.

Fig. 4

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Mean concentration of heavy metals (mg/kg) in the tissue of infected P. erumei with Hysterothylacium spp. larvae and non-infected fish

Discussion

The term parasite is usually associated with adverse effects on the host, such as disease and pathogenicity. Parasites, on the other hand, can be helpful to their hosts on occasion. The parasites can reduce heavy metal concentrations in their hosts' tissues in this way. Metal concentrations in some helminths are substantially higher than in their hosts, according to (Galli et al. 1998; Sures 2001; Williams & MacKenzie 2003; Malek et al. 2007). While helminth parasites, particularly acanthocephalans, have been used as valuable bio-indicators of heavy metal contamination in aquatic environments (Sures & Siddall 1999; Nachev et al. 2013; Sures 2004b; Mehana et al. 2020), studies on the role of parasitic nematodes in metal monitoring are limited. Furthermore, most accessible nematode articles focus on the accumulation potential of adult parasites (Nachev et al. 2013), In contrast, larval nematodes are less intensively investigated, and knowledge on their accumulation capacity is a scientific gap.

Ascaridoid nematodes (family Anisakidae), which have over 200 species worldwide, are suitable for environmental monitoring because of their wide range, high accumulation capacity, and adaptive flexibility against adverse conditions (Køie et al. 1995; Sures 2003). Hysterothylacium (Nematoda: Anisakidae) uses fish as intermediate and definitive hosts (Dural et al. 2011; Khaleghzadeh-Ahangar et al. 2011; Abdel-Ghaffar et al. 2015). These parasitic nematodes reside as larvae and adults in the body cavities, mesenteries, and intestines of marine fishes (Balbuena et al. 2000; Klimpel et al. 2006). One of the major hosts of this helminth is P. erumei, a commercially valuable fish in the Persian Gulf. As a demersal fish that feeds on invertebrates and benthic plants, it has a higher potential for accumulating metal pollution, which is frequently related to sediments (Saei-Dehkordi et al. 2010; Hosseini et al. 2016). In Iran, the level of heavy metals in the muscles of P. erumei fish in the Persian Gulf was explored by Alinejad et al. (2015), Hosseini et al. (2016), and Gholamhosseini et al. (2018). However, up until now, no research has been done in this area on the association between P. erumei fish, parasites, and heavy metal contamination. Our study focused on larvae of Hysterothylacium in the P. erumei intestine and provides new information on the heavy metal concentrations in the tissues of P. erumei as fish host and Hysterothylacium spp. larvae as its parasites in the Persian Gulf.

From the standpoint of food hygiene, studies of heavy metal absorption by parasites of fishes are considerable. In this study, comparisons of element concentrations between Hysterothylacium spp. larvae and P. erumei muscles revealed that elements of Fe, Cu, Zn, Ni, Cr, and Hg were found to be greater in parasites, whereas elements of As, Cd, and Pb were detected to be higher in host muscles. The accumulation of essential elements (Fe, Cu, Zn) and non-essential ones (Ni) was significantly higher in the Hysterothylacium spp. larvae, which are consistent with Mazhar et al., 2014. According to a study done in the eastern coastal waters of the South China Sea Hysterothylacium reliquens has a strong tendency to accumulate important elements such as Fe, Cu, Zn, Ni, and Mn (Abdel-Ghaffar et al. 2015). Toxic metals (Pb, Cd, Hg, and As) accumulate in high concentrations in Hysterothylacium spp. compared to fish tissues, based on some research (Khaleghzadeh-Ahangar et al. 2011; Mazhar et al. 2014). Despite this, our data revealed that the toxic element (As) was found in considerably higher concentrations in host tissues. This inconsistency may be explained by differences in the research area or various hosts.

From a public health perspective, it is essential to determine the concentration of heavy metals in fish caught. Comparing element concentrations in infected and non-infected fish revealed that infected hosts with parasites had lower Fe, Zn, As, and Hg concentrations, while non-infected hosts had lower Ni, Cd, and Pb concentrations. The concentrations of heavy metals in the muscles of infected and non-infected hosts, however, did not change significantly. Only As element showed a significantly lower concentration in the infected hosts' muscles. This nematode is vital because it absorbs many fish arsenic, making fish meat healthier than fish without parasites. Arsenic is a toxic metalloid element found in water, air, and soil and can cause cancer in humans (Ratnaike 2003). This finding for Hysterothylacium spp. was also reported by Khaleghzadeh-Ahangar et al. (2011), who found no significant variations in cadmium and lead concentrations between the infected and non-infected host's tissues. Meanwhile, according to numerous studies, non-infected hosts had significantly much greater levels of heavy metals than infected hosts (Sures et al. 1999; Bergey et al. 2002; Dural et al. 2011).

Conclusion

This study investigated the concentration of heavy metals in host fish and their parasites since there is a lack of information about the toxicological accumulation of heavy metals in aquatic organisms and their parasites in the Persian Gulf. Our findings highlight the importance of Hysterothylacium spp. larvae as a heavy metals bio-indicator. The concentrations of Fe, Cu, Zn, and Ni in Hysterothylacium spp. larvae were higher than those in P. erumei muscles. In addition, infected hosts had lower As levels in their muscles than non-infected ones. This nematode seems to be able to use more in environmental studies to monitor heavy metals pollution. Because of their function as heavy metals filters, these parasites benefit to their hosts' health.

Acknowledgements

The authors appreciate the Vice-Chancellor of Research, Bushehr University of Medical Sciences, Bushehr, Iran, for the collaboration and financial support of this research. We also acknowledge the Shiraz University of Medical Sciences for their collaboration in providing laboratory equipment to conduct this study.

Authors' contribution

B.S: Experimental work and Manuscript preparation. S.M.S: Study design and Manuscript review. G.M: Data analysis. M.R: Study supervision and Manuscript editing. All authors read and approved the final manuscript.

Declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper

Ethics approval

This Research was approved by the Ethics Committee of Bushehr University of Medical Sciences (IR.BPUMS.REC.1395.121).

Footnotes

Publisher's Note

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

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