Lipid contents in different tissues of Indonesian coelacanth
Lipid contents varied in different tissue of Indonesian coelacanth, with liver tissue having a higher percentage of lipid content (40.0%) than muscle (3.3%) and ovary (0.8%) (Table 1). Compared with a previous study on coelacanth fish from Comoro Island (Hale et al. 1991), the lipid content was comparable in the liver but relatively low in the muscle tissue (32% and 16% reported in the Comoro coelacanth specimen, respectively). These results agree with another study that deep-sea fish have a high percentage of lipid in their liver, where the metabolism and storage of xenobiotic compounds occur.
Contamination status of PCBs
PCBs were detected in all the tissues of Indonesian coelacanth analyzed. Concentrations of total 209 PCBs (Σ209 PCBs), PCB homologs, indicator PCB congeners (in-PCBs: CB-28, -52, -101, -118, -138, -153, and − 180), and dioxin-like PCBs (dl-PCBs) are summarized in Table 1 (the data of individual PCB congeners is shown in Table S2, Supporting Information). The total accumulation of Σ209 PCBs in the different tissue of Indonesian coelacanth revealed that liver tissue had higher concentrations than muscle and ovary on a wet weight basis. Meanwhile, as the liver has greater lipid content than muscle and ovary, lipid-normalized concentrations of PCBs become lower in the liver than in muscle and ovary tissues. Concentrations of Σ209 PCBs in the liver, muscle, and ovary tissue of Indonesian coelacanth were 300, 2600, and 1800 ng g− 1 lw (mean: 1600 ng g− 1 lw), with concentrations of total in-PCBs ranging between 100 ng g− 1 lipid lw in the liver tissue and 870 ng g− 1 lipid lw in the muscle tissue (mean: 550 ng g− 1 lw). The concentration of dl-PCBs was from 17 ng g-1 lw in the liver to 120 ng g− 1 lw in ovary tissue. In this study, predominant congeners of dl-PCBs in all tissues were mono-ortho PCBs up to 99%, with concentrations ranging from 9.0 ng g− 1 lw to 95 ng g− 1 lw. In contrast, non-ortho dl-PCBs represented only a small fraction of the total dl-PCBs (Table 1).
The concentrations of PCBs detected in the present study were higher than those reported in the female coelacanth fish from Comoro Island, with the concentration in liver tissue was 280 ng g− 1 lw, muscle tissue was 240 ng g− 1 lw, and kidney tissue was 880 ng g− 1 lw (Hale et al. 1991). However, the detailed number of congeners and concentration of individual congeners are not reported. Therefore, this comparison did not provide significant insight regarding pollution status in coelacanth fish. On the other hand, it is of interest to note that the range of PCB concentrations in the tissues of Indonesian coelacanth (300–2600 ng g− 1 lw) as deep-sea fish seems to be comparable to those reported in coastal fish from polluted bays such as Jakarta Bay, Indonesia, with total concentrations of ∑62PCBs in marine fish between 260 − 2700 ng g− 1 lw, or other location in Indonesia such as Lada Bay (32 − 360 ng g− 1 lw), Cirebon coastal water (27–560 ng g− 1 lw), and Lampung Bay (9.7–94 ng g− 1 lw) (Sudaryanto et al. 2007).
Relatively high PCB concentrations in deep-sea fishes have been widely reported in deep-sea fauna compared to biota living on the surface (De Brito et al., 2002; Takahashi, 2014). The deep-sea organism can accumulate POPs through several mechanisms, such as vertical transport of contaminated organic matter as sea snow from the surface to the deep-sea ecosystem and through the pelagic-benthic coupling food web (Takahashi et al., 2014; Cui et al., 2020). In contrast, the high concentration of PCBs in the current study might be due to the feeding behavior of Indonesian coelacanth as a piscivorous predator (Saruwatari et al. 2019). Coelacanth usually hunts other small fishes near the surface between approximately 200 m below the surface to about 500 m in depth (Fricke and Hissmann 2000). Therefore, further study should investigate the accumulation of PCBs and other pollutants in the prey of Indonesian coelacanth and their ecosystems.
In comparison with other deep-sea fishes around the Pacific and Indian Ocean (Table S3, Supporting Information), the range of PCB concentrations in Indonesian coelacanth (300–2600 ng g− 1 lw) was higher than in deep-sea fishes from the East China Sea (36 − 1400 ng g− 1 lw) (Tanabe et al. 2005), Suruga Bay (450 − 1900 ng g− 1 lw) and Tosa Bay (not detected (nd) − 1600 ng g− 1 lw), Japan (Takahashi et al., 1998; Takahashi et al., 2001, respectively), Western North Pacific (off Tohoku) (nd − 2200 ng g− 1 lw) (De Brito et al. 2002a); and Sulu Sea (19 − 110 ng g− 1 lw) (Ramu et al. 2006). However, the concentrations in Indonesian coelacanth appear to be lower than those reported in snub-nosed eels from Western North Pacific (6700 ng g− 1 lw) (De Brito et al. 2002a) and around 25 fold lower than those in the liver of bonnethead sharks from Florida (880 − 68900 ng g− 1 lw) (Weijs et al. 2015). On the other hand, it should be considered that variation/uncertainty in comparison of the data of total PCBs between studies is due to several factors such as the number of targeted congeners, tissue samples, and different analytical techniques (Bartalini et al. 2019).
Although concentrations of dl-PCBs in the tissue of Indonesian coelacanth only represented a small fraction of the total Σ209PCBs from 3–5%, dl-PCBs have dioxin-like toxicity due to their ability to bind aryl hydrocarbon (Ah) receptor and cause disorders in various organs systems (Huang et al. 2020). To evaluate the potential toxicological effect of dl-PCBs in Indonesian coelacanth, we calculated toxic equivalent (TEQ) values based on the concentrations of dl-PCBs detected in the coelacanth tissues and TCDD equivalency factors (TEF) adopted by WHO (1998) for fish (Van Den Berg et al., 1998). The calculated TEQ of dl-PCBs in the tissues of Indonesian coelacanth ranged from 0.0035 to 0.12 pg TEQ/g ww and from 0.29 to 0.47 pg TEQ/g lw. These TEQ values were below threshold levels for early life stage mortality in fish, with the tissue-residue benchmark for TCDD TEQ ranging from 57 to 699 TCDD TEQ/g lipid (Steevens et al. 2005). A comparison with other studies shows that the levels of TEQs in this study are lower than those in other deep-sea fishes from the Mediterranean Sea (rough snout grenadier: 44 pg TEQ/g ww; hollow snout grenadier: 20 pg TEQ/g ww) (Storelli et al. 2009), the Mediterranean Sea (ghost sharks: 0.48 pg TEQ/g ww; skates: 0.33 pg TEQ/g ww) (Storelli et al. 2004), but comparable with those found in the Avilés Canyon, Atlantic Ocean (pelagic fish: 0.054 pg TEQ/g ww, demersal fish: 0.017 pg TEQ/g ww) (Romero-Romero et al. 2017).
Profile of PCB congeners
It is important to note that PCB congeners in coelacanth tissue are unique and isomer-specific accumulation. In general, the highest proportion of PCB homolog was penta-CBs (mean: 34%), followed by hexa-CBs (30%) and tetra-CBs (27%). The liver performed as the predominant tissue for tetra-CBs accumulation with a proportion of 38%. In comparison, the muscle showed a high affinity for penta-CBs with a relative proportion of around 37%. The highest proportion of hexa-CBs was found in ovary tissue, with a relative proportion accounting for 40% of total PCBs (Fig. 3). Additionally, the higher proportion of individual congeners to total PCBs in the liver, muscle, and ovary are CB-52 (16%), CB-99 (11%), and highly recalcitrant congeners (CB-153, 12%), respectively (Fig. 4). Contribution of dl-PCBs to the total PCBs from 3 to 5%, with CB-118 in mono-ortho dl-PCBs being the predominant compound with a percentage of 2.0 − 3.6% and followed by CB-105 (0.50–0.88%). Profile differences between the tissue of Indonesian coelacanth can be affected by various factors, including properties of individual congeners, the relative proportion of lipid class, or lipid mobilization between tissue compartments (Kainz and Fisk 2009).
A previous study on Latimeria chalumnae, a relative species of Indonesian coelacanth, reported a specific class and proportion of lipid in the tissue; liver tissue has a high proportion of triacylglycerol (TAG), around 78%, followed by wax ester (WE) 8.2%, and polar lipids 9.1%. In comparison, muscle tissue has a large percentage of WE more than 90% (Nevenzel et al. 1966). Although the proportion of TAG in liver tissue is high enough to accumulate high chlorinated PCBs, WE and polar lipid also have another task on tissue distribution of PCBs. Notably, the predominant proportion of WE with a long carbon chain (C32-C36) in the Latimeria muscle/adipose tissue may cause the species-specific tissue distribution of PCBs in this fish. Although TAG is one of the non-polar lipids, long-chain WE have a more stable and non-polar nature than the other lipids. Therefore, it can be considered that long-chain WE tend to retain more “non-polar” congeners (i.e., high chlorinated PCBs) than TAG and polar lipids, which constitute liver lipids predominantly. In addition, Nevenzel et al. (1966) reported that monounsaturated fatty acid, C 18:1 (60%), is a dominant TAG component in the Latimeria liver tissue. Although high proportions of TAG/polar lipids in liver tissue and long-chain WE in muscle/ovary tissue are expected in Indonesian coelacanth, further research on lipid character in this species is necessary to determine the relationship between lipid characters and tissue-specific accumulation of PCBs.
Besides, it should be noted that a relatively less proportion of hexa-CBs (19%) in the liver tissue of Indonesian coelacanth (Fig. 3) is different from other reported studies with hexa-CBs as predominant homolog in the liver tissue of deep-sea biotas such as found in deep-sea shark (63–64%) (Storelli et al., 2005), Mediterranean slimehead and blackfin sorcerer from Mediterranean Seas (56% and 55%, respectively) (Storelli and Perrone, 2010), deep-sea fishes from the North Atlantic and Northeast Pacific regions (Froescheis et al. 2000) or even epibenthic deep-sea invertebrate from two of the deepest hadal trenches (Mariana Trench in the North Pacific and Kermadec Trench in the South Pacific) (Jamieson et al. 2017) and the northern Gulf of Mexico (Lawson et al. 2021). This may reflect different PCB exposure and/or contamination sources in Indonesian deep waters from those in other locations. For example, technical PCB mixtures having lower chlorinated congeners as major components (e.g., Arochlor 1242 and Kanechlor 300) may be used in Indonesia or surrounding areas/countries. A previous study of PCBs on Indonesian sediments from the Surabaya coastal area (Ilyas et al., 2011) reported that some of the sampling stations were characterized by lower chlorinated PCB congeners, which are similar to the profiles of Arochlor 1242 or Kanechlor 300/400. In addition, profiles of PCB residues in deep-sea coelacanth may reflect a historical pattern of PCBs preserved in the deep-water environment rather than weathering pattern (i.e., the dominance of recalcitrant and high chlorinated congeners) of PCBs shown in coastal/terrestrial food webs. Comprehensive monitoring is necessary to explain the pattern of PCBs in the habitat and food preference of Indonesian coelacanth.
Contamination status of BFRs
PBDEs were detected in the all-tissue samples at relatively low concentrations. Among 36 PBDEs analyzed in this study, only nine congeners (i.e., BDE-47, -49, -66, -100, -126, 153, -154, -196, and − 203) was detected in liver tissue with a concentration between 0.051 and 1.9 ng g− 1 lw (total: 3.9 ng g− 1 lw), three congeners (i.e., BDE-47, -49, and − 99) in muscle tissue with a concentration between 0.63 and 4.5 ng g− 1 lw (total: 6.1 ng g− 1 lw), and only one congener (BDE-47) was detected in ovary tissue with a concentration of 4.5 ng g− 1 lw. Among four other BFRs, only BTBPE was detected in liver and muscle tissue at a concentration of 1.1 and 3.6 ng g− 1 lw, respectively (Table 2). Lower detectable PBDEs and other BFRs in the coelacanth tissue might be influenced by several factors, including low levels of BFRs in Indonesian offshore/deep waters, physicochemical properties, and/or biotransformation potential of these compounds (Ma et al. 2013).
Compared to deep-sea fishes from other locations, particularly from the recent 5 years (2015 − 2020) (Table S2), the average concentration of Σ10PBDEs (4.8 ± 1.1 ng g− 1 lw) in Indonesian coelacanth was comparable to those in fish from the Sulu Sea (1.5 ng g− 1 lw) (Ramu et al. 2006), Western North Pacific (1.3–8.5 ng g− 1 lw) (Takahashi et al. 2010), and Mediterranean deep-sea fish (C. coelorynchus) with Σ8PBDE ranged from 3.2–7.0 ng g− 1 lw (Covaci et al. 2008). Also, our results are still lower than those reported for deep-sea fishes from North-West Mediterranean (average Σ14PBDE: 62 ± 29 ng g− 1 lw in A. antennatus and 190 ± 27 ng g− 1 lw in L. lepidion) (Koenig et al. 2013) and other deep-sea fish from the Mediterranean (T. trachyrinchus) with concentration ranged from 12–27 ng g− 1 lw (Covaci et al. 2008).
BTBPE, on the other hand, was detected at a relatively low concentration compared with other studies. For example, a previous study reported that BTBPE was detected in Greenland shark liver with a concentration of 8.1 ng g− 1 lw and the liver of juvenile sole with concentrations ranging from 5.3 − 40.2 ng g− 1 lw (Strid et al., 2013; Munschy et al., 2011). Considering the lower concentration of other BFRs in the present study, the previous research suggested that it was due to limited volume production and just introduced to the market (Karlsson et al. 2006). Consequently, this compound might be less exposed to biota and the environment.
Despite no statistical information on the number of technical BDE mixtures imported and no production of these compounds in Indonesia, the environmental impact of PBDEs released maybe not be negligible due to the significant accumulation of electrical and electronic waste (e-waste) from households in Indonesia, estimating up to 622,000 tonnes in 2025 (Andarani and Goto 2014). Another study also calculates the growth rate of e-waste in Indonesia as around 15% annually and is estimated to reach 487,416 tons by 2028 (Santoso et al. 2019). Therefore, even though the concentration of PBDEs in this study is still lower and with more undetectable congeners, future mitigation is needed to monitor the impact of an increasing number of e-waste and the potential impact of informal recycler of e-waste in Indonesia.
Congener profiles of BFRs
An interesting finding on PBDEs distribution pattern was observed in tissues of Indonesian coelacanth. In this study, ten congeners (BDE-47, -49, -66, -99, -100, -126, 153, -154, -196, and − 203) out of 36 PBDE congeners and one of four other BFRs were detected in tissues of Indonesian coelacanth. All detected congeners were mainly lower brominated congeners (tetra- to hexa-BDEs), with BDE-47 and BDE-99 as the highest proportion of total PBDEs, up to 75% and 20%, respectively. Predominant congeners in the present study resemble those reported elsewhere in many aquatic ecosystems worldwide. For example, BDE-47 was detected in up to 50% of total PBDEs in the liver of Mediterranean deep-sea fish and up to 71% of the ΣPBDE concentration in the amphipods from Mariana Trench and Kermadec Trench (Covaci et al., 2008; Jamieson et al., 2017). The prevalence of BDE-47 and BDE-99 in the organism tissues may be related to continual release from the application of commercial Penta-BDEs such as DE-71 and Bromkal 70-5DE in such regions (Huang et al. 2020). BDE-47 and BDE-99 are the main components of penta-BDE, a commercial PBDE mixture commonly used to manufacture various refractory and flame-retardant materials for various electronic equipment.
Moreover, other potential explanations for the observed high proportion of lower brominated congeners (di- to tetra-BDEs) might be a sign of the metabolism capacity of Indonesian coelacanth on PBDEs. A previous study reported that experiments with some fish species, including Japanese medaka, fathead minnows, and Cyprinus carpio, showed debromination of higher brominated congener (BDE-99, BDE-183, and BDE-209) into lower brominated congener (Stapleton et al., 2004; Benedict et al., 2007; Noyes et al., 2011; Q et al., 2013). Thus, these experiment results might be potential explanations for the relatively low composition of higher brominated such as BDE-183 and BDE-209 in deep-sea fish (Koenig et al., 2013). Food web transfer is another mechanism for more detectable lower brominated PBDEs in Indonesian coelacanth. Based on biomagnification factor calculation, lower brominated PBDEs, including tri- to hexa-BDE congeners, have high biomagnification potential to transfer through the food web (Shaw et al. 2012).