Distribution of trace element concentrations in invertebrate species collected from Tokyo Bay, Japan

ABSTRACT

Three bivalves, Cyclina sinensis (n=6), Crassostrea gigas (n=7), and Mactra veneriformis (n=6), and three crustaceans, Hemigrapsus penicillatus (n=5), Macrophthalmus japonicus (n=5), and Pyrhila pisum (n=5), were collected at Haneda in June 2019. In July 2019, M. veneriformis (n=5) and M. japonicus (n=3) were collected at Kasai. Concentrations of 34 trace elements were analyzed in muscles and internal organs: Li, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, Ga, As, Se, Rb, Sr, Y, Mo, Cd, In, Sn, Sb, Cs, Ba, La, Ce, Gd, Pt, Tl, Pb, and Bi. C. sinensis and M. veneriformis accumulate elements higher in internal organs than muscles. But C. gigas indicates a different accumulation from other bivalves. The strength of hypoxia tolerance may be related to the difference in element distribution among the tissues because C. gigas is exposed to air at low tide, but the other bivalves are not. Moreover, C. sinensis and M. veneriformis accumulated the elements abundant in sediment such as rare earth elements. However, C. gigas accumulated different elements from other bivalves: Cu, Zn, Cd, and Pb. The effect of habitat, in or above the sediment, seemed related to the accumulated element composition. While crustaceans accumulated elements higher in the hepatopancreas than in muscles. In crustaceans, detritus-eating or carnivorous feeding may have affected the accumulated element composition. Most elements, except Mg, K, Ca, and Sr, in the hepatopancreas of H. penicillatus and M. japonicus had higher concentrations than in P. pisum. The detritus-eating in crustaceans was likely to result in accumulating elements with microplastics as one of their origins, e.g., Al, Mn, Co, Cu, Ba, and Pb. Moreover, all invertebrates in Haneda accumulated higher concentrations of Zn than in other studies—likely due to industrial wastes and tires disposed of in Haneda. Additionally, most high-toxicity element concentrations in Kasai were at similar or higher levels than in Haneda. Thallium was only detected in Kasai and was higher than in other studies. Thus, different trace element distributions were suggested among sites in Tokyo Bay.

INTRODUCTION

Trace elements are detected at lower levels in the tissues of living organisms. Essential elements and nonessential elements (e.g., As, Cd, Hg, and Pb) accumulate in the body after uptake (Gu et al., 2018). Nonessential elements are not necessary and have high toxicity for living organisms (Takekawa et al., 2002). Additionally, essential elements are also toxic to the organism in excess, and Cr, Co, and Ni, although essential elements are highly toxic when consumed in excess (Hajimohammadjafartehrani et al., 2019; Ahmad et al., 2022; van den Brule et al., 2022). Trace elements have two origins: natural and anthropogenic. The main anthropogenic sources are industrial activities, agriculture, domestic wastewater, mining, and nearby transportation (Mathivanan and Rajaram, 2014; Velusamy et al., 2014; Radomyski et al., 2018; Ezemonye et al., 2019). These elements flow into aquatic ecosystems via sewage and runoff (Liu et al., 2018; Ezemonye et al., 2019) and enter aquatic organisms mainly by feeding (Zhao et al., 2012; Jayaprakash et al., 2015; Jitar et al., 2015; Gu et al., 2018). Trace elements are difficult for living organisms to degrade and remain in various environments for a long period, which is a major problem on the global scale due to bioaccumulation from the predation of organisms in higher trophic levels (Widdows et al., 1995; Duman et al., 2007; Ho et al., 2012; Zahra et al., 2014; Chen et al., 2018; Liu et al., 2018; Sobihah et al., 2018). Aquatic organisms such as molluscan bivalves and crustaceans have differences in the accumulation of elements (Liu et al., 2018; Satheeswaran et al., 2019). Understanding the relationships between trace element accumulation and the behavior of aquatic organisms, habitat, and feeding behavior, is essential to elucidating the causes of trace element contamination.

Estuaries and coastal areas in aquatic ecosystems have unique ecosystems such as tidal flats, which are primary production sites for aquatic organisms (Barbier et al., 2011; Zohary and Gasith, 2014; Zhao et al., 2020). Therefore, pollution in these sites can reduce the productivity of marine organisms and lead to death (Balls et al., 1997; Chapman and Wang, 2001; Satheeswaran et al., 2019). However, coastal and estuarine areas are frequently polluted by the influx of trace elements from surrounding land and rivers (Satheeswaran et al., 2019). Tokyo Bay in Japan is surrounded by Tokyo, Chiba, and Kanagawa prefectures. Tokyo Bay is a closed bay with a narrow mouth and shallow water, making it difficult to exchange water with the open sea (Wakabayashi, 2000) and many rivers flow into the deep part of the bay via the major urban areas of the neighboring prefectures. The residential area around Tokyo Bay has one of the largest population densities in Japan as well as many active industrial areas. Therefore, the deep part of Tokyo Bay is considered to have a particularly large influx of trace elements and serious pollution. Additionally, since the period of high economic growth after World War II, land has been reclaimed in the coastal areas. Therefore, natural tidal flats decreased and the retention of pollution became more serious by decreasing their self-cleaning action (Ogura and Takada, 1995; Wakabayashi, 2000). In recent years, artificial tidal flats have been formed, and thus recovering the purification effect of tidal flats is expected. However, the inflow of trace elements from the river and the surrounding land is still considered sufficient to cause environmental pollution.

In this study, several invertebrates were collected from tidal flats in the deep part of Tokyo Bay to evaluate the distribution of trace elements. The purpose of this study is threefold: (I) to analyze biological tissues such as muscles and internal organs to evaluate the distribution of trace elements among tissues; (II) to gain an understanding of interspecies differences in accumulation and elucidate the causes; and (III) to assess pollution at Haneda by comparison with Kasai, different sites in Tokyo Bay, and other studies.

MATERIALS AND METHODS

The sampling sites are shown in Fig. 1: Haneda, Ota Ward, Tokyo; and Kasai (Tokyo Sea Life Park), Edogawa Ward, Tokyo. Haneda, located at the estuary of the Tamagawa River, is one of the few natural tidal flats in Tokyo Bay. This site is adjacent to Haneda International Airport, one of the largest airports in Japan. Various factories are located in Kawasaki City, Kanagawa Prefecture, on the opposite shore. The Tamagawa River has a total length of 138 km and watershed area of 1,240 km², runs from the western part of Tokyo and passes through its urban areas (Zheng et al., 2014). Around the Tamagawa River, the population is 11.77 million and population density is 3,400 people/km² (average in Japan is 334 people/km²), therefore, a heavy anthropogenic load on the river is expected (Takii and Fukui, 1991; Zheng et al., 2014; Horii et al., 2022). Furthermore, since 1960, the traffic network around Tokyo has developed and the traffic volume around the Tamagawa River has increased (Kuno et al., 1997, 1999; Zheng et al., 2002). Kasai is an artificial tidal flat. Tokyo Sea Life Park (Kasai) is registered under the Ramsar Convention only in Tokyo. Kasai is located between the estuaries of the Kyu-Edogawa and Arakawa Rivers. This area has much industrial activity and busy roads like Haneda. The Kyu-Edogawa River flows along the border of Chiba and Tokyo Prefectures. The population surrounding the river is 1.41 million and watershed area is 200 km². The Arakawa River has 2,940 km² basin area and 9.76 million basin population, and it flows through the main parts of Saitama and Tokyo. In terms of size, these two rivers should have a smaller load than the Tamagawa River. However, both rivers pass through the areas than the Tamagawa River, so there are different pollution concerns for these sites.

Fig. 1

Sampling site, Haneda and Kasai in Tokyo Bay, Tokyo (Image source: Geographical Survey Institute)

Some invertebrates were selected as biological samples: molluscans (bivalves) and crustaceans (crabs). Bivalves accumulate metals in organic and inorganic forms through filtration feeding from the surrounding environment (Liu et al., 2018), and consequently have been used in many studies as indicators of environmental pollution in aquatic ecosystems (Huang et al., 2007; Bartolomé, et al., 2010; Liu et al., 2018). Crustaceans are not commonly used as indicators of environmental pollution. However, some crustaceans accumulate some trace elements in high concentrations (Liu et al., 2018). In this study, bivalves Cyclina sinensis (n=6), Crassostrea gigas (n=7) and Mactra veneriformis (n=6) and crustaceans Hemigrapsus penicillatus (n=5), Macrophthalmus japonicus (n=5) and Pyrhila pisum (n=5) were collected at Haneda in June 2019. In July 2019, M. veneriformis (n=5) and M. japonicus (n=3) were collected at Kasai. Each species was placed in a polyethylene bag and transported to the laboratory in a cooler box with coolants. Mud adhering to the invertebrates was immediately washed off with ion-exchange water in the laboratory and then the specimens were stored in a freezer (−20°C) until analysis. The frozen specimens were thawed at room temperature and washed with ion-exchange water and Milli-Q water again. The cleaned samples were subjected to biometric measurements using calipers and electronic balance. Shell height, length, and weight were measured in bivalves, and weight in crustaceans. For C. gigas, only soft tissues were weighed. All bivalves were separated into muscles and internal organs (nonmuscle parts) and crustaceans were separated into muscles and hepatopancreas by scalpel. However, only the hepatopancreas was analyzed in P. pisum in Haneda and M. japonicus in Kasai because muscle amounts were small. The samples were divided into Petri dishes for each individual and tissue, weighed by electronic balance, and oven-dried (90°C, 24 h). After determining dry weight, all samples were powdered using a ceramic mortar and pestle. Then, about 0.100 g of the powdered sample was weighed into a vial tube. The dry weight (<0.100 g) of the sample was used for all quantities. 61% HNO₃, 2.0 ml was added to the dried sample, and digestion was conducted (200 W, 20 min) using a microwave oven. Digestion samples were filtered through ADVANTEC 5C filter paper and transferred to polypropylene test tubes and diluted about 250 times with Milli-Q water. The diluted solution was weighed to determine the dilution factor and used for analysis. Thirty-four trace elements (Li, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, Ga, As, Se, Rb, Sr, Y, Mo, Cd, In, Sn, Sb, Cs, Ba, La, Ce, Gd, Pt, Tl, Pb, and Bi) concentrations were analyzed by inductively coupled plasma mass spectrometry (ICP-MS; Agilent 7500cx) with ¹⁰³Rh as the internal standard. When the element concentration was under the detection limit, the instrumental detection limit of ICP-MS was used for analysis as the limit of detection for convenience. The instrumental detection limit was the estimated standard deviation of 10 measurements of 5% HNO₃ multiplied by three. Elements below the detection limit for all individuals were excluded from statistical analysis. The instrumental detection limit of all elements is indicated in Table 1. Additionally, the accuracy of the methods was assessed using standard reference materials NIST 1577b and SRM1577b (National Institute of Standards and Technology) (Horai et al., 2006; Suzuki et al., 2006).

Table 1 The instrumental detection limit in this study of inductively coupled plasma mass spectrometry (Agilent 7500cx)

Element name	Li	Na	Mg	Al	K	Ca	V	Cr	Mn	Fe	Co	Ni	Cu	Zn	Ga	As	Se
LOD	0.00006	0.003	0.0004	0.0002	0.005	0.00005	0.001	0.001	0.001	0.0001	0.002	0.0004	0.005	0.001	0.0006	0.0001	0.00001

Element name	Rb	Sr	Y	Mo	Cd	In	Sn	Sb	Cs	Ba	La	Ce	155Gd	157Gd	Pt	Tl	Pb	Bi
LOD	0.0009	0.001	0.002	0.0007	0.00008	0.003	0.0007	0.0007	0.002	0.0003	0.004	0.004	0.0009	0.0009	0.001	0.005	0.005	0.004

Statistical analysis used R version 3.6.0. and R studio. All analysis was nonparametric. For statistical analysis, heat maps and principal component analysis (PCA) were used to identify characteristics of the distribution of elements and individuals. Kruskal–Wallis test was used to test differences among the three groups. As a post hoc test, the Dunn test was used for crustaceans. The Mann–Whitney test was used for bivalves since only C. gigas had one more individual than other bivalves. Critical p-value was p<0.05.

RESULTS AND DISCUSSION

ELEMENT CONCENTRATIONS IN INVERTEBRATE TISSUES AND SPECIES IN HANEDA

Trace element concentrations in muscles and internal organs in invertebrates are shown in Tables 2 and 3, respectively.

Table 2 Trace element concentrations (μg/g d.w.) in the muscles of invertebrates collected from Haneda and Kasai in June and July 2019, respectively

Sample name	n	Sampling site		Li	Na	Mg	Al	K	Ca	V	Cr	Mn	Fe	Co	Ni	Cu	Zn	Ga	As
Cyclina sinensis	6	Haneda	Range	0.507–0.848	17,700–31,000	4,830–6,810	23.2–63.9	2,570–4,770	1,760–2,390	0.691–1.23	1.18–3.05	5.70–14.3	159–250	1.41–3.78	8.43–30.9	<0.005	164–292	0.0432–0.0569	4.52–7.08
		Estuary of Tama River	Average±SD	0.631±0.118	24,000±4,080	5,700±601	42.6±15.5	4,070±758	2,110±220	0.941±0.192	1.79±0.61	9.89±2.72	215±28	2.52±0.72	18.3±6.7	<0.005	210±41	0.0494±0.0051	5.67±0.88
Crassostrea gigas	7	Haneda	Range	<0.00006–0.996	3,720–5,690	1,680–1,990	102–434	3,610–5,640	217–5,420	0.473–1.13	<0.001–1.34	32.7–72.2	311–705	0.246–0.618	0.708–1.59	132–451	1,700–5,050	<0.0006–0.134	5.59–9.61
		Estuary of Tama River	Average±SD	0.788±0.115	4,760±622	1,830±99	247±94	4,860±599	2,590±1,680	0.776±0.198	1.11±0.19	54.3±13.5	504±108	0.441±0.123	1.16±0.28	324±119	3,140±1,080	0.0962±0.0232	7.56±1.12
Mactra veneriformis	6	Haneda	Range	0.562–0.854	18,700–26,600	5,350–6,230	11.7–72.4	2,230–5,470	1,700–7,600	0.630–1.39	1.46–76.6	10.1–22.1	197–517	0.383–0.916	<0.0004–5.18	<0.005	<0.001–194	<0.0006–0.0620	3.03–5.81
		Estuary of Tama River	Average±SD	0.694±0.105	23,500±2,981	5,830±344	38.8±21.7	4,290±1,150	3,280±1,990	1.03±0.29	19.8±26.3	15.0±4.2	302±102	0.692±0.226	4.32±0.68	<0.005	138±33	0.0512±0.0080	4.32±0.83
Hemigrapsus penicillatus	5	Haneda	Range	<0.00006–0.803	9,640–11,900	2,170–3,650	23.2–130	4,510–5,860	1,260–5,930	<0.001–0.309	<0.001	11.3–105	50.8–324	<0.002–0.466	0.746–8.86	99.7–131	175–454	<0.0006	4.52–10.5
		Estuary of Tama River	Average±SD	0.803	10,900±790	2,760±542	66.8±41.6	5,310±456	3,040±1,620	0.263±0.061	<0.001	60.2±32.1	198±96	0.377±0.066	3.18±2.94	111±11	247±105	<0.0006	7.44±2.19
Macrophthalmus japonicus	5	Haneda	Range	<0.00006–1.98	8,100–19,800	3,910–6,080	194–572	5,100–6,600	2,860–7,430	0.578–1.45	0.851–1.28	23.0–191	391–883	0.186–0.768	0.651–2.00	84.3–116	220–296	<0.0006–0.162	1.48–2.91
		Estuary of Tama River	Average±SD	1.24±0.47	12,500±3,920	5,370±754	380±122	5,650±507	5,400±1,480	0.937±0.307	1.08±0.18	82.9±60.2	579±166	0.399±0.213	1.51±0.48	104±11	252±25	0.117±0.032	2.40±0.51
Mactra veneriformis	5	Kasai	Range	0.689–1.02	8,410–13,900	3,280–4,800	211–743	737–1,030	389–1,070	0.656–1.54	0.523–1.32	36.9–373	<0.0001–745	1.30–3.59	<0.0004	<0.005	<0.001–133	0.0702–0.216	4.70–10.3
		Tokyo Sea Life Park	Average±SD	0.872±0.125	10,100±1,980	4,020±519	406±207	904±117	744±249	1.04±0.33	0.894±0.313	155±122	560±148	2.07±0.80	<0.0004	<0.005	113±14	0.132±0.054	6.50±1.97

Sample name	n	Sampling site		Se	Rb	Sr	Y	Mo	Cd	Sn	Sb	Cs	Ba	La	Ce	155Gd	157Gd	Tl	Pb
Cyclina sinensis	6	Haneda	Range	9.22–12.5	2.20–3.82	76.0–99.4	0.195–0.547	<0.0007–0.298	<0.00008–0.0740	<0.0007	<0.0007	<0.002	1.40–2.03	0.464–1.01	0.416–0.957	0.252–0.571	0.0589–0.154	<0.005	<0.005
		Estuary of Tama River	Average±SD	10.6±1.1	3.21±0.52	83.3±8.0	0.348±0.123	0.271±0.020	0.0740	<0.0007	<0.0007	<0.002	1.66±0.22	0.660±0.204	0.622±0.185	0.368±0.114	0.0973±0.0317	<0.005	<0.005
Crassostrea gigas	7	Haneda	Range	3.52–7.15	3.92–6.02	10.4–133	0.202–0.474	<0.0007	1.70–2.78	<0.0007	<0.0007–7.17	<0.002–0.0933	0.295–1.61	0.134–0.412	0.216–0.656	<0.0009–0.0984	<0.0009–0.0896	<0.005	0.914–1.64
		Estuary of Tama River	Average±SD	5.52±1.03	5.32±0.66	69.5±39.9	0.304±0.089	<0.0007	2.15±0.41	<0.0007	3.73	0.0675±0.0147	0.737±0.388	0.237±0.102	0.393±0.169	0.0766±0.0213	0.0700±0.0188	<0.005	1.28±0.30
Mactra veneriformis	6	Haneda	Range	6.21–56.9	3.81–7.32	50.4–121	<0.002–0.245	<0.0007–0.244	<0.00008–0.155	<0.0007	<0.0007	<0.002	0.891–2.34	<0.004–0.392	<0.004–0.408	<0.0009–0.348	<0.0009–0.0598	<0.005	<0.005–0.444
		Estuary of Tama River	Average±SD	28.9±21.8	5.16±1.42	77.7±22.8	0.158±0.056	0.243	0.147	<0.0007	<0.0007	<0.002	1.54±0.43	0.303±0.061	0.303±0.074	0.223±0.078	0.0470	<0.005	0.434
Hemigrapsus penicillatus	5	Haneda	Range	1.62–3.68	4.09–5.19	156–631	<0.002	<0.0007	<0.00008	<0.0007	<0.0007	<0.002	2.73–10.0	<0.004	<0.004	<0.0009	<0.0009	<0.005	<0.005–0.721
		Estuary of Tama River	Average±SD	2.22±0.77	4.74±0.41	324±168	<0.002	<0.0007	<0.00008	<0.0007	<0.0007	<0.002	5.38±2.52	<0.004	<0.004	<0.0009	<0.0009	<0.005	0.721
Macrophthalmus japonicus	5	Haneda	Range	3.08–3.49	4.09–5.66	308–716	0.131–0.304	<0.0007	<0.00008	<0.0007	<0.0007	<0.002–0.0906	4.01–13.3	0.167–0.352	0.329–0.825	<0.0009–0.103	<0.0009–0.0722	<0.005	0.472–1.06
		Estuary of Tama River	Average±SD	3.30±0.15	4.58±0.56	543±131	0.204±0.058	<0.0007	<0.00008	<0.0007	<0.0007	0.0764	8.50±3.20	0.247±0.064	0.561±0.166	0.0941	0.0599	<0.005	0.719±0.214
Mactra veneriformis	5	Kasai	Range	1.65–3.23	1.42–1.60	63.4–160	0.576–1.04	0.207–0.271	0.209–0.540	<0.0007	<0.0007	0.0111–0.0955	2.81–7.37	0.515–1.04	0.552–1.04	0.136–0.240	0.109–0.196	<0.005–0.0153	<0.005–3.15
		Tokyo Sea Life Park	Average±SD	2.53±0.56	1.52±0.06	109±37	0.803±0.162	0.235±0.025	0.341±0.117	<0.0007	<0.0007	0.0469±0.0285	4.96±1.66	0.775±0.174	0.849±0.188	0.192±0.036	0.159±0.031	0.0135±0.0018	1.28±1.10

Table 3 Trace element concentrations (μg/g d.w.) in the internal organs of invertebrates collected from Haneda and Kasai in June and July 2019, respectively

Sample name	n	Sampling site		Li	Na	Mg	Al	K	Ca	V	Cr	Mn	Fe	Co	Ni	Cu	Zn	Ga	As
Cyclina sinensis	6	Haneda	Range	0.688–1.06	12,600–29,900	4,830–6,810	102–431	3,160–4,820	1,760–2,390	1.40–2.35	1.64–3.09	10.8–21.8	325–719	0.775–3.83	3.16–15.8	<0.005	98.6–148	0.0853–0.180	6.77–10.1
		Estuary of Tama River	Average±SD	0.879±0.114	21,900±6,690	5,700±601	306±134	4,090±709	2,110±220	1.77±0.37	2.34±0.52	16.4±3.6	513±139	1.82±1.00	8.18±3.99	<0.005	121±16	0.139±0.034	8.46±1.04
Crassostrea gigas	7	Haneda	Range	0.184–0.856	3,080–4,710	1,370–1,920	40.5–360	4,850–5,340	69.3–1,020	0.389–1.25	<0.001–1.97	9.45–78.0	199–680	0.252–0.611	0.314–0.999	121–289	1,480–2,620	<0.0006–0.119	6.37–13.4
		Estuary of Tama River	Average±SD	0.383±0.244	3,990±536	1,650±185	151±114	5,120±178	423±385	0.705±0.289	0.998±0.531	47.5±25.1	358±169	0.429±0.136	0.647±0.246	190±49	2,020±376	0.0725±0.0342	11.0±2.3
Mactra veneriformis	6	Haneda	Range	<0.00006–2.36	19,900–25,400	5,200–6,630	708–2,070	2,240–5,330	2,460–10,400	2.44–4.43	3.44–39.9	27.2–78.6	1,240–3,010	1.05–1.82	<0.0004–7.70	<0.005–47.9	<0.001–238	<0.0006–0.580	2.31–6.87
		Estuary of Tama River	Average±SD	1.83±0.32	21,600±1,850	5,850±607	1,330±504	4,010±1,080	5,520±3,440	3.22±0.82	10.6±13.2	44.5±17.4	1,880±792	1.32±0.27	5.68±1.47	35.3	184±49	0.401±0.104	4.88±1.48
Hemigrapsus penicillatus	5	Haneda	Range	1.46–16.9	5,820–12,800	2,760–5,070	715–8,630	1,960–3,080	1,610–5,220	1.87–18.8	1.34–11.6	55.7–388	1,240–12,500	1.61–7.27	4.81–18.6	203–382	124–203	0.238–3.04	4.98–7.57
		Estuary of Tama River	Average±SD	7.88±5.15	9,120±2,470	4,220±873	4,130±2,730	2,570±371	3,870±1,240	9.73±5.87	7.34±4.08	215±110	6,370±3,860	3.93±1.90	11.3±4.8	311±68	160±30	1.44±0.97	6.36±0.89
Pyrhila pisum	5	Haneda	Range	0.559–2.03	11,600–18,500	3,540–8,810	3,540–8,810	3,820–5,710	2,390–13,700	<0.001–3.08	<0.001–1.35	21.5–68.2	166–1,880	1.15–1.90	1.54–3.60	36.9–78.5	132–214	<0.0006–0.314	5.52–10.1
		Estuary of Tama River	Average±SD	1.19±0.64	14,600±2,350	5,660±2,260	5,660±2,260	4,780±612	6,420±4,080	1.64±0.84	1.01	43.4±18.0	810±582	1.64±0.30	2.51±0.74	53.0±14.2	167±30	0.206	7.09±1.57
Macrophthalmus japonicus	5	Haneda	Range	0.359–8.57	10,600–16,300	4,220–5,900	4,220–5,990	2,660–4,390	2,880–4,550	0.875–10.0	<0.001–7.84	228–367	277–6,580	0.330–3.40	0.730–6.81	153–604	123–244	<0.0006–1.55	3.98–8.55
		Estuary of Tama River	Average±SD	3.93±3.18	13,200±1,850	4,850±570	4,850±570	3,330±619	3,850±671	4.88±3.43	4.36±2.69	310±59	3,030±2,410	1.71±1.07	3.69±2.12	379±186	180±52	1.10±0.33	6.28±1.89
Mactra veneriformis	5	Kasai	Range	0.605–2.55	7,290–14,000	4,060–4,790	237–2,090	783–1,120	564–1,060	1.06–4.41	0.661–3.78	70.5–752	395–2,500	1.92–4.06	<0.0004–7.33	<0.005–21.1	114–161	0.103–0.642	8.72–12.3
		Tokyo Sea Life Park	Average±SD	1.15±0.72	9,830±2,330	4,400±274	831±668	1,000±122	871±181	2.03±1.23	1.59±1.14	293±263	1,050±768	2.97±0.76	7.33	21.1	131±17	0.278±0.196	10.3±1.3
Macrophthalmus japonicus	3	Kasai	Range	1.47–6.75	7,690–12,600	5,460–7,520	2,070–9,280	2,940–3,810	3,800–9,290	3.38–14.5	2.55–12.0	232–442	1,850–8,040	1.11–3.78	3.34–11.2	203–288	126–175	0.461–2.23	7.34–8.92
		Tokyo Sea Life Park	Average±SD	4.22±2.16	10,400±2,040	6,760±922	5,850±2,950	3,510±403	5,950±2,390	8.85±4.54	7.55±3.88	315±91	5,210±2,550	2.74±1.17	7.48±3.22	254±37	144±22	1.40±0.73	8.13±0.65

Sample name	n	Sampling site		Se	Rb	Sr	Y	Mo	Cd	Sn	Sb	Cs	Ba	La	Ce	155Gd	157Gd	Tl	Pb
Cyclina sinensis	6	Haneda	Range	9.96–15.2	2.73–4.11	38.2–99.5	0.280–0.539	0.374–0.706	0.0956–0.191	0.0509–0.207	<0.0007	<0.002–0.0607	0.788–1.51	0.409–0.882	0.488–1.05	0.241–0.486	0.0896–0.195	<0.005	<0.005–1.27
		Estuary of Tama River	Average±SD	13.2±1.6	3.50±0.53	66.5±23.2	0.401±0.101	0.493±0.106	0.135±0.040	0.107±0.057	<0.0007	0.0555±0.0055	1.23±0.24	0.566±0.170	0.765±0.182	0.333±0.090	0.139±0.035	<0.005	0.951±0.196
Crassostrea gigas	7	Haneda	Range	3.21–7.90	5.15–6.36	6.59–29.7	0.133–0.420	<0.0007	0.777–2.44	<0.0007–0.193	<0.0007–3.02	0.0258–0.0797	0.337–0.998	0.0742–0.314	0.101–0.556	<0.0009–0.0843	<0.0009–0.0787	<0.005	0.798–1.50
		Estuary of Tama River	Average±SD	6.50±1.57	5.72±0.48	14.6±8.9	0.240±0.103	<0.0007	1.53±0.56	0.169±0.031	3.02	0.0445±0.0178	0.620±0.221	0.174±0.081	0.285±0.157	0.0521±0.0197	0.0536±0.0156	<0.005	1.19±0.27
Mactra veneriformis	6	Haneda	Range	<0.00001–11.2	3.23–4.49	61.2–163	0.776–1.58	<0.0007–0.543	<0.00008–0.316	<0.0007–0.527	<0.0007	<0.002–0.212	2.46–5.84	0.931–1.69	1.57–3.24	0.745–1.55	0.306–0.674	<0.005	<0.005–4.42
		Estuary of Tama River	Average±SD	5.51±2.88	4.10±0.45	108±36	1.16±0.28	0.448±0.081	0.261±0.043	0.273±0.150	<0.0007	0.144±0.042	4.15±1.31	1.28±0.28	2.32±0.63	1.15±0.31	0.477±0.122	<0.005	2.98±0.89
Hemigrapsus penicillatus	5	Haneda	Range	3.58–8.27	4.11–12.0	151–533	0.363–3.24	<0.0007–1.97	0.357–0.685	<0.0007–0.675	<0.0007	0.154–1.29	2.80–24.1	0.386–5.40	0.809–10.7	0.100–1.19	0.0897–1.05	<0.005	1.16–9.42
		Estuary of Tama River	Average±SD	5.27±1.68	7.64±2.78	408±137	1.82±1.05	1.88	0.536±0.116	0.426±0.215	<0.0007	0.703±0.389	14.4±7.3	2.52±1.74	5.27±3.48	0.616±0.384	0.545±0.340	<0.005	5.54±2.95
Pyrhila pisum	5	Haneda	Range	4.51–7.52	4.62–5.70	273–1,330	<0.002–0.605	<0.0007	0.210–1.19	<0.0007	<0.0007	<0.002–0.157	2.65–11.8	<0.004–0.940	<0.004–1.97	<0.0009–0.190	<0.0009	<0.005	<0.005–2.18
		Estuary of Tama River	Average±SD	6.32±1.09	5.17±0.44	656±380	0.295±0.221	<0.0007	0.673±0.312	<0.0007	<0.0007	0.0882±0.0503	5.95±3.49	0.376±0.328	0.775±0.696	0.190	<0.0009	<0.005	1.49±0.68
Macrophthalmus japonicus	5	Haneda	Range	4.93–6.70	2.69–8.29	306–548	0.120–2.09	<0.0007–0.843	0.214–1.42	<0.0007–0.431	<0.0007	<0.002–0.860	8.86–24.9	0.183–2.82	0.254–5.84	<0.0009–0.687	<0.0009–0.607	<0.005	0.503–5.97
		Estuary of Tama River	Average±SD	6.13±0.64	5.63±2.18	431±84	0.989±0.746	0.843	0.832±0.486	0.297±0.104	<0.0007	0.475±0.293	14.5±5.6	1.29±0.97	2.58±2.08	0.397±0.222	0.439±0.119	<0.005	2.91±2.12
Mactra veneriformis	5	Kasai	Range	3.38–5.45	1.44–2.38	96–124	0.827–2.55	0.377–0.720	0.330–1.05	<0.0007–2.51	0.0165–0.0392	0.0345–0.252	5.32–6.36	0.641–2.48	0.766–3.31	0.215–0.651	0.183–0.584	0.0106–0.0320	0.753–5.57
		Tokyo Sea Life Park	Average±SD	4.40±0.77	1.70±0.34	115±10	1.62±0.58	0.525±0.113	0.513±0.270	1.02±0.75	0.0262±0.0079	0.106±0.079	5.82±0.43	1.40±0.62	1.76±0.86	0.443±0.147	0.406±0.137	0.0181±0.0077	1.86±1.86
Macrophthalmus japonicus	3	Kasai	Range	4.51–6.43	3.87–7.37	368–870	1.02–3.97	<0.0007	0.452–0.568	<0.0007–0.417	<0.0007	0.314–1.10	11.9–21.3	0.714–3.15	1.60–7.14	0.248–0.980	0.216–0.911	<0.005	1.54–6.25
		Tokyo Sea Life Park	Average±SD	5.69±0.84	5.44±1.45	565±219	2.79±1.27	<0.0007	0.505±0.048	0.300	<0.0007	0.753±0.327	16.3±3.9	2.01±1.00	4.60±2.29	0.673±0.310	0.622±0.295	<0.005	4.52±2.11

Element distributions in both tissues of bivalves differed among species. For example, 15 elements (Li, Al, V, Mn, Fe, Ga, As, Y, Mo, Cd, Sn, Cs, Ce, ¹⁵⁷Gd, and Pb) concentrations in C. sinensis and M. veneriformis were higher in internal organs than in muscles. However, in C. gigas, a few elements had higher concentrations in internal organs than in muscles: K, As, Se, Rb, and Sn. Concentrations of Li, Al, V, Mn, Fe, Ga, As, Se, Mo, and Cd in internal organs compared to muscles and Ni, Zn, and Ba in muscles of C. sinensis compared to internal organs were significantly higher (p<0.05). Similarly, Li, Al, V, Mn, Fe, Co, Ga, Y, Sn, Ba, La, Ce, ¹⁵⁵Gd, and ¹⁵⁷Gd concentrations in internal organs were significantly higher than in muscles, and Se concentration in M. veneriformis muscles was significantly higher than in internal organs (p<0.05). The concentration of As in internal organs was significantly higher in C. gigas, than in muscles, and Ca, Ni, Se and Cs concentrations in muscles were significantly higher than in internal organs (p<0.05). So, in terms of element concentration, the elements showing significant differences among the tissues were fewer in C. gigas than in C. sinensis and M. veneriformis. Differences in hypoxia tolerance due to differences in their habitats may be related. Oysters frequently experience hypoxia and anoxia when exposed to air at low tide because they are attached to bedrock (Greenway and Storey, 1999; Lenihan et al., 2001; Ivanina et al., 2011). Oyster Crassostrea virginica can maintain metabolism until 5% oxygen concentration (Ivanina et al., 2011). In C. gigas, anaerobic metabolism is induced under anoxic conditions (Meng et al., 2018). The bivalves in this study differed in the amount of oxygen they supplied. Because of living in sediment, both C. sinensis and M. veneriformis can take in oxygen from surface seawater and pore-water within sediment (Ding et al., 2020, 2021). However, C. gigas can take oxygen only from surface water (Cho et al., 2021). The amount of oxygen intake of these two bivalves is expected to be higher than that of C. gigas. Differences in hypoxia tolerance, body size, and morphological defenses occur between intertidal and subtidal populations of aquatic invertebrates (Altieri, 2006; Weihe and Abele, 2008; Botta et al., 2014; Meng et al., 2018) and the distribution of trace elements among the tissues may also be affected by hypoxia tolerance. The result implied that trace element distribution to muscles may be higher in species with superior anaerobic metabolism. The previous study (Bagwe et al., 2015) reports a decrease in the upper critical temperature due to 50 μg/L Cd concentration. The Cd concentrations in tissues of all C. gigas exceeded 50 μg/kg with range of 34–56 times higher in muscles and 16–49 times higher in internal organs. However, most muscles of C. sinensis and M. veneriformis were below the Cd detection limit. Furthermore, Cd concentrations in C. sinensis and M. veneriformis internal organs were approximately 2–3 times higher than 50 μg/kg. Therefore, C. gigas in Haneda may be more affected by the transfer of trace elements with anaerobic metabolism than other bivalves.

Most element concentrations in crustaceans were found to be higher in the hepatopancreas than in the muscles. Potassium concentration in muscle was significantly higher in both species (p<0.05). Concentrations of Al, V, Fe, Co, Ni, Cu, and Se in H. penicillatus and Mn, Co, Cu, As, and Se in M. japonicus were significantly higher in hepatopancreas than in muscles (p<0.05). Lithium, Cr, Ga, Y, Cd, Sn, Cs, La, Ce, ¹⁵⁵Gd, and ¹⁵⁷Gd in H. penicillatus and Cd, Sn, Cs, ¹⁵⁵Gd, and ¹⁵⁷Gd in M. japonicus were likely to be detected in the hepatopancreas. The crustaceans indicate a tendency to transfer elements to muscles less frequently. Furthermore, lanthanides in rare earth elements (REEs) were detected at higher concentrations in hepatopancreas. Lanthanum, Ce, and Gd have high toxicity in the human body (USEPA, 2012), and some REEs show plant toxicity (Ding et al., 2005). The REEs taken into bodies permeate cell membranes and distribute to each cell organelle after binding to erythrocytes (Chen et al., 2001; Wu et al., 2002; Wei et al., 2013; Bonnail et al., 2017). In crustaceans, REEs mainly accumulate in the hepatopancreas. This result indicated the metabolic distribution to muscles occurred only slightly. Additionally, Cd concentration in the hepatopancreas of crustaceans is higher than those in muscles. This result is consistent with previous findings that Ucides cordatus transports Cd frequently to the gill and hepatopancreas (Ortega et al., 2017).

All the analyzed bivalves are detritus-eating. However, habitat differs with C. sinensis and M. veneriformis living in sediment, and C. gigas attached to bedrock. Thus, C. gigas is considered less affected by sediment among these species.

Cobalt, Ni, Sr, Y, Mo, Ba, La, Ce, ¹⁵⁵Gd, and ¹⁵⁷Gd concentrations in muscles and Na, Co, Ni, Se, and Mo concentrations in internal organs of C. sinensis were the highest among the bivalves. Especially, Co, Ni, Y, Ba La, Ce, and ¹⁵⁵Gd concentrations in muscles and Na, Co, Ni, Se and Mo in internal organs were significantly higher in the three bivalves (p<0.05). Molybdenum exceeded the detection limit only in all C. sinensis in tissue. Cobalt and Ni concentrations of C. sinensis were reported to be higher than those in C. gigas (Ito et al., 2013), and these results were similar. Magnesium, Ca, V, Cr, and Se concentrations in muscles and Li, Mg, Al, Ca, V, Cr, Fe, Ga, Sr, Y, Sn, Cs, Ba, La, Ce, ¹⁵⁵Gd, and ¹⁵⁷Gd in internal organs of M. veneriformis were the highest among the bivalves. Concentrations of Mg, Cr, and Se in muscles and Li, Mg, Al, Ca, V, Cr, Fe, Ga, Sr, Y, Ba, La, Ce, ¹⁵⁵Gd, and ¹⁵⁷Gd in internal organs were significantly higher than in other bivalves (p<0.05). Trace metals are likely to stick to the mucus in M. veneriformis gills and are not easily expelled once taken into the body (Okutani and Soyama, 1987). Additionally, M. veneriformis generally has longer contact times of soft tissues with the external environment because of the tendency not to close its shells completely (Miyake, 1953). Therefore, M. veneriformis stores substances for a longer period than other bivalves, and the element concentrations in its internal organs were higher than in muscles. The other characteristic of element accumulation in M. veneriformis internal organs was that all REE concentrations were the highest among the bivalves. The C. sinensis accumulated REEs primarily in muscles, with no discernible difference in concentrations between the tissues. All REEs concentrations of M. veneriformis were significantly higher in internal organs than muscles.

Concentrations of Li, Al, K, Mn, Fe, Cu, Zn, Ga, As, Rb, Cd, Cs, and Pb in muscles and of K, Mn, Cu, Zn, As, Rb, and Cd in internal organs of C. gigas were the highest among the three bivalves. Especially, concentrations of Al, Mn, Fe, Zn, As, and Rb in muscles and of K, Zn, As, Rb, and Cd in internal organs were significantly higher than in other bivalves (p<0.05). Additionally, Cu, Cd, and Pb concentrations in muscles were below the detection limit in most C. sinensis and M. veneriformis; but all were above the detection limit in C. gigas. Copper, Zn, Cd, and Pb are known to undergo metabolic reactions and detoxification by binding to metallothionein (MT) (Dunn et al., 1987; Viarengo and Nott, 1993; Tanguy and Moraga, 2001; Meistertzheim et al., 2009). Genes that induce MT expression to reduce metallurgical stress are present in C. gigas (Tanguy and Moraga, 2001). Oyster Saccostrea glomerata was reported to induce high amounts of MT in the presence of high Cd and Zn concentrations (Yingprasertchai et al., 2019). In C. gigas, MT increased the uptake of Cd and Zn and the other elements easily induced by MT, such as Cu and Pb (Yingprasertchai et al., 2019). Additionally, MT is highly expressed in mammals and aquatic crustaceans under hypoxic conditions (Kojima et al., 2009; Felix-Portillo et al., 2014). The same gene for MT expression is found in several aquatic invertebrates (Mao et al., 2012). Therefore, the accumulation of Cu, Zn, Cd, and Pb in C. gigas was thought to be associated with MT. Furthermore, the effects of hypoxic stress might induce more MT in C. gigas at Haneda, possibly explaining why MT-related elements were at higher concentrations in C. gigas than in the other bivalves.

The accumulation of these elements in bivalves differed between species of living in (C. sinensis and M. veneriformis) and above sediment (C. gigas). Species living in sediment take food and oxygen from surface water as well as pore-water in sediment, while C. gigas takes in only surface water (Cho et al., 2021). So, it is expected that the effect of sediment in C. sinensis and M. veneriformis is higher than in C. gigas. Additionally, the amount of oxygen supplied may be related to differences in distribution of elements among bivalves as well as in tissues. Oysters and mussels are widely used as useful indicators in many environmental surveys, and species living in sediment are more useful for assessment of sediment contamination compared to oysters.

In hepatopancreas, H. penicillatus accumulated the greatest variety of these elements among the three crustaceans, and also had the highest concentrations of Li, Al, V, Cr, Fe, Co, Ni, Ga, Rb, Y, Mo, Sn, Cs, La, Ce, ¹⁵⁵Gd, ¹⁵⁷Gd, and Pb. Vanadium, Ni, Y, and La concentrations significantly differed among the three species (p<0.05). Hemigrapsus penicillatus usually lives under the bedrock (Ogura and Kishi, 1985; Kurihara et al., 1989) and eats mainly algae such as green laver, diatoms, and larvae of the same species (Okamoto and Kurihara, 1989). Especially, H. penicillatus larvae are highly selected and preferentially consumed because of containing large amounts of organic matter, while diatoms and green laver, containing less organic matter than H. penicillatus larvae, have been reported to be consumed in large quantities for ingestion of a sufficient amount of organic matter (Okamoto and Kurihara, 1989). Much algae attached to rocks are found near the habitat of H. penicillatus. Since all H. penicillatus growth stages feed on attached algae, the elements in H. penicillatus likely derive from the algae. Aluminum, Cr, Co, Ni, Rb, Sn, and Pb concentrations, all high-toxicity elements, were highest in H. penicillatus among the three crustaceans and may be absorbed by attached algae in Haneda. Moreover, REE concentrations in H. penicillatus hepatopancreas were the highest among the three crustaceans. The REEs are mainly contained in the earth’s crust and are expected to be more abundant in sediments than in seawater. The three crustaceans are always in contact with sediment. Therefore, each of their primary foods may be related to the differences in REEs accumulations: M. japonicus eats detritus in surface sediments (Ono, 1995), while P. pisum eats small bivalves and carcasses (Kobayashi, 2013). Only H. penicillatus mainly eats larvae of the same species (Okamoto and Kurihara, 1989). The larvae of H. penicillatus are also thought to eat mainly the algae and attached film on bedrock (Okamoto and Kurihara, 1989). Therefore, in H. penicillatus, bioaccumulation of trace elements to the adult may occur by preying on the larvae of the same species that have already accumulated trace elements in their bodies from algae and attached film. Additionally, the algae have a high accumulating capacity for REEs and use as the absorber of REEs from water (Hao et al., 1997; Ramasamy et al., 2019; Cao et al., 2021). So, the primary food and feeding habitat of H. penicillatus, algae, and bioconcentration by eating the larvae of the same species, may be related to inducing the highest accumulation of REEs and some high toxicity elements. Among the three crustaceans, Mn, Cu, Zn, Cd, and Ba concentrations in M. japonicus were the highest; this species digs a hole in sediment for protection and emerges from its burrow at low tide to eat the detritus from surface sediments (Ono, 1995; Yamoti et al., 1997). So, the elements in M. japonicus are related to the origin of detritus. Surface detritus contain excrement from oysters (Forrest and Creese, 2006; Yamamoto et al., 2010; Jonathan et al., 2017), and high concentrations of Mn, Cu, Zn, and Cd in M. japonicus suggest the mixing of oyster excrement in detritus because these element concentrations were also the highest in C. gigas among bivalves. Additionally, Al, Mn, Co, Cu, Ba, and Pb are all reported to be present in plastics (Holmes et al., 2012; Turner and Holmes, 2015; Brennecke et al., 2016; Yamaguchi, 2016; Godoy et al., 2019), and their concentrations were higher in the hepatopancreas of H. penicillatus and M. japonicus than P. pisum. Some plastic wastes drift into Haneda and plastic wastes become fragmented into microplastic (MP) by physicochemical factors and are taken into aquatic organisms (Godoy et al., 2019; Cho et al., 2021). Because it contains trace elements originally and also adsorbed from the environment, MP is associated with trace elements in marine organisms (Holmes et al., 2012; Wang et al., 2019; Dong et al., 2020). Most MP settles on sediment (Ding et al., 2021) and H. penicillatus and M. japonicus have a common food of algae, attached to (Okamoto and Kurihara, 1989) or settled on the bedrock (Ono, 1995). The detritus- and algae-feeding crustaceans take up MP by mistake and are more affected than carnivores.

Among the three crustaceans, Na, Mg, K, Ca, As, Se, and Sr concentrations were highest in P. pisum. Many element concentrations in the hepatopancreas of P. pisum were below the detection limit. Pyrhila pisum is carnivorous, feeding mainly on small bivalves or open shell carcasses (Kobayashi, 2013), and does not eat detritus derived from vascular plants and bivalves with hard shells or that burrow deep in sediment (Kobayashi, 2013). One of the shallow burrowing and fragile shell bivalves in Haneda is M. veneriformis and this is likely one of the main foods of P. pisum. In fact, all the elements with the highest concentrations in P. pisum among the three crustaceans also had their highest concentrations in M. veneriformis among the bivalves. The transfer of elements to P. pisum from M. veneriformis may occur. Several elements had significant differences between P. pisum and the other crustaceans: V, Ni, Cu, Y, and La (p<0.05). No elements significantly differed between H. penicillatus and M. japonicus. The main foods of H. penicillatus and M. japonicus are similar but that of P. pisum is totally different. The differences in foods among crustaceans contribute to element distributions.

Heatmap analysis was used to compare the distribution of trace elements in the internal organs of all invertebrates (Fig. 2). A cluster of most H. penicillatus and M. japonicus occurred in the left-most part of the X-axis and included most elements. The statistical analysis supports that many elements tended to accumulate in H. penicillatus. The elements that occur in plastics such as Al, Mn, Co, Cu, Ba, and Pb were in this cluster. The statistical analysis supports the effect of MP ingestion in two crustaceans and possibly that they were more severely affected than bivalves. However, a few H. penicillatus and M. japonicus individuals formed the other cluster. Crustaceans control element concentrations by molting and accumulate high concentrations of some elements in the hepatopancreas before molting (Nędzarek et al., 2019). The time course from molting differs among individuals, resulting in no consistent accumulation characteristics among crustaceans. On the other hand, P. pisum formed the other cluster characterized by elements not common with those in H. penicillatus and M. japonicus. The differences in element distribution according to food type were supported by statistical analysis. Furthermore, some common elements in M. veneriformis were shown in P. pisum. Heatmap analysis supported that M. veneriformis was one food of P. pisum. In bivalves, all C. gigas formed one cluster characterized by K, Zn, As and Cd–both Zn and Cd are associated with MT. The characterization of elements bound and detoxified by MT, such as Zn and Cd (Yingprasertchai et al., 2019), were observed in Fig. 2, the statistical analysis supports a stronger effect of MT in C. gigas than in other invertebrates. But Cu and Pb were characteristic of H. penicillatus and M. japonicus, and this may be associated with the fact that MP settles onto the sediment (Ding et al., 2021). The C. sinensis and M. veneriformis formed separate but adjacent clusters. The elements characteristic of C. gigas had no commonality with these clusters. The statistical analysis supports differences in element distribution in bivalves depending on habitat. Moreover, some elements were common with those in H. penicillatus and M. japonicus. The similarity of element distributions between bivalves and crustaceans due to the common habitat of sediment was also shown. Additionally, the commonly characterized elements by C. sinensis and M. veneriformis are only Na and Mg. Differences in distribution between C. sinensis and M. veneriformis were shown.

Fig. 2

Result of heatmap analysis using the element concentrations in internal organs of three bivalve species, Cyclina sinensis, Crassostrea gigas, and Mactra veneriformis, and three crustacean species, Hemigrapsus penicillatus, Pyrhila pisum, and Macrophthalmus japonicus (collected from Haneda in June 2019)

COMPARING INVERTEBRATE ELEMENT CONCENTRATIONS WITH OTHER STUDIES

Comparisons of element concentrations with previous studies are shown in Tables 4 and 5. Aluminum concentration in M. veneriformis at Haneda was higher than in most other studies and at similar levels to a heavily polluted area in Tanzania (Rumisha et al., 2012). In C. sinensis, Al was also at higher concentrations than most other studies. The concentrations in C. gigas at Haneda were likely similar to or higher than those found in Italy because they were 3–16 times higher than wet weight concentrations (Burioli et al., 2017). Aluminum is a nonessential element and has potential toxicity for the liver in fish (d’Haese and De Broe, 1994; Authman, 2011). Moreover, Cr had the highest concentration in M. veneriformis at Haneda, and Cr concentration in C. sinensis was higher than for bivalves in India (Satheeswaran et al., 2019). However, the concentration in other invertebrates was similar to those of other studies. The Fe and Mn concentrations in invertebrates in Haneda were lower than in most previous studies. The Ni concentration in C. gigas in Haneda is estimated to be similar to or lower than for C. gigas in Italy (Burioli et al., 2017). However, Ni concentrations in C. sinensis, M. veneriformis and H. penicillatus in Haneda were higher than in most previous studies. Some species living in sediment in Haneda, especially bivalves, may be polluted by Ni. Cobalt concentration in C. sinensis was higher than in most previous studies. All crustaceans in Haneda had higher Co concentrations than in other studies. Cobalt contamination in crustaceans at Haneda may be greater than in other areas. Copper and Zn pollution in C. gigas has been previously found (Burioli et al., 2017; Jonathan et al., 2017; Kunene et al., 2021). Copper concentration in C. gigas in Haneda is estimated to be similar to or lower than in C. gigas in Italy (Burioli et al., 2017). Moreover, Cu concentration in C. sinensis and M. veneriformis in Haneda were mostly under the detection limit, but a few individuals had levels as high as in other studies. All crustaceans in Haneda had higher Cu concentrations than other studies. So, Cu pollution in crustaceans may occur. However, Zn concentration in all invertebrates in Haneda was much higher than in other studies. The C. gigas soft tissue turns blue when Zn concentration exceeds 500–700 mg/kg dry wt. (Kunene et al., 2021). Zn concentration in C. gigas in Haneda was 3–10 times higher than that for adverse effects (Kunene et al., 2021). The high Zn concentration in invertebrates in Haneda is caused by the inflow of industrial waste and MP, and also by the release of Zn by degradation and leaching from tires dumped in large amounts in Haneda. Zinc is a particularly high component of tires (Klöckner et al., 2021). Moreover, Haneda Airport and the road leading to it are located near the sampling site, and dust from worn car tires may flow into the sampling site with runoff. Zinc is essential for both humans and invertebrates, but it is acutely toxic to fish (Kodama et al., 1982) and increases mortality Pecten maximus mortality by weakening shell strength (Stewart et al., 2021). Shell strength of bivalves is important for protection against predators, and weak shells increase the risk of predation. Therefore, Zn contamination in the Haneda ecosystem is considered particularly dangerous. Arsenic, Se, Cd, and Pb concentrations in invertebrates at Haneda were mostly similar to other studies. However, most previous studies were based on the analysis of contaminated sites. So, contamination of comparable areas is continuing at Haneda.

Table 4 Comparison of trace element concentrations (μg/g) in bivalves, using results of this study and previous studies

Sample name	site	n	Organ	Al		Cr		Mn		Fe		Co		Ni		Cu		Note	Referrence
				Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD
This Study
Cyclina sinensis	Haneda (Esutuary of Tama River)	6	Muscle	23.2–63.9	42.6±15.5	1.18–3.05	1.79±0.61	5.70–14.3	9.89±2.72	159–250	215±28	1.41–3.78	2.52±0.72	8.43–30.9	18.3±6.7	<0.005	<0.005		—
			Others	102–431	306±134	1.64–3.09	2.34±0.52	10.8–21.8	16.4±3.6	325–719	513±139	0.775–3.83	1.82±1.00	3.16–15.8	8.18±3.99	<0.005	<0.005		—
Crassostrea gigas	Haneda (Esutuary of Tama River)	6	Muscle	102–434	247±93.9	0.804–1.34	1.11±0.19	32.7–72.2	54.3±13.5	311–705	504±108	0.246–0.618	0.441±0.123	0.708–1.59	1.16±0.29	132–451	324±119		—
			Others	40.5–360	151±114	0.431–1.97	0.998±0.531	9.45–78.0	47.5±25.1	199–680	358±169	0.252–0.611	0.429±0.136	0.314–0.999	0.647±0.246	121–289	190±49		—
Mactra veneriformis	Haneda (Esutuary of Tama River)	7	Muscle	11.7–72.4	38.8±21.7	1.46–76.6	19.8±26.3	10.1–22.1	15.0±4.2	197–517	302±102	0.383–0.916	0.692±0.226	3.53–5.18	4.32±0.68	<0.005	<0.005		—
			Others	708–2,720	1,330±504	3.44–39.9	10.6±13.2	27.2–78.6	44.5±17.4	1,240–3,010	1,880±792	1.05–1.82	1.32±0.27	4.23–7.70	5.68±1.47	<0.005–47.9	35.3		—
Mactra veneriformis	Kasai (Tokyo Sea Life Park)	5	Muscle	211–743	406±207	0.523–1.32	0.894±0.313	36.9–373	155±122	365–745	560±148	1.30–3.59	2.07±0.80	<0.0004	<0.0004	<0.005	<0.005		—
			Others	237–2,090	831±668	0.661–3.78	1.59±1.14	70.5–752	293±263	395–2,500	1,050±768	1.92–4.06	2.97±0.76	<0.0004–7.33	7.33	<0.005–21.1	21.1		—
Previous Research
Crassostrea gigas	La Pitahaya channel (Mexico)	20	Soft Tissue	—	—	0.33–104	22.29±30.23	—	—	—	—	—	—	1–42.33	9.41±11.33	26.33–85.33	63.37±31.72		Jonathan et al., 2017
	Caorle (Italy, Open Sea)	6	Soft Tissue	11.2–18.8	15.07±3.22	0.072–0.097	0.08±0.01	5.9–9.6	7.95±1.51	59.7–102.7	72.02±18.85	—	—	0.14–0.2	0.17±0.02	27.6–54.0	36.38±10.44	Wet weight	Burioli et al., 2017
	Cervia (Italy, Open Sea)	6	Soft Tissue	38.5–99.6	61.33±21.27	0.22–0.45	0.32±0.08	6.1–9.3	7.97±1.13	64.2–163.5	103.40±38.54	—	—	0.23–0.41	0.33±0.06	89.8–163.8	130.02±31.78	Wet weight	Burioli et al., 2017
	Monfalcone (Italy, Gulf)	3	Soft Tissue	11.0–22.1	15.97±5.64	0.15–0.22	0.19±0.04	5.9–8.0	6.70±1.13	42.1–48.0	44.83±2.97	—	—	0.12–0.18	0.15±0.03	110.4±127.3	119.17±8.47	Wet weight	Burioli et al., 2017
	Muggia (Italy, Gulf)	3	Soft Tissue	38.6–57.1	47.30±9.30	0.28–0.42	0.37±0.08	0.1–0.8	0.37±0.38	65.8–122.1	88.10±29.92	—	—	0.26–0.48	0.39±0.11	315.2–491.2	412.10±89.34	Wet weight	Burioli et al., 2017
	Giulianova (Italy, Gulf)	6	Soft Tissue	51.5–111.4	71.27±23.78	0.16–0.35	0.23±0.07	7.9–81.8	22.00±29.36	75.3–143.1	98.25±25.14	—	—	0.14–0.21	0.18±0.03	675.1–1219.9	946.40±193.14	Wet weight	Burioli et al., 2017
	Porto Garibaldi (Italy, Harbor)	3	Soft Tissue	16.2–21.8	18.47±2.95	0.096–0.26	0.17±0.08	5.5–7.8	6.43±1.21	41.1–42.7	42.17±0.92	—	—	0.14–0.27	0.20±0.07	52.7–59.1	55.13±3.46	Wet weight	Burioli et al., 2017
	Caleri (Italy, Lagoon)	9	Soft Tissue	12.1–88.55	56.20±22.81	0.09–0.27	0.21±0.05	8.3–13.6	11.35±1.90	53.6–104.3	81.20±15.52	—	—	0.19–0.31	0.24±0.04	4.4–65.0	40.60±22.98	Wet weight	Burioli et al., 2017
	Cavallino-Trepoti (Italy. Lagoon)	12	Soft Tissue	8–77.1	31.30±24.85	0.11–1.1	0.36±0.31	—	—	75.8–607.8	283.63±155.96	—	—	0.14–0.77	0.29±0.19	47.9–133.2	76.90±23.47	Wet weight	Burioli et al., 2017
	Chioggia (Italy, Lagoon)	3	Soft Tissue	38.4–45.7	41.27±3.89	0.15–0.24	0.20±0.05	5.3–6.7	6.17±0.76	72.7–92.6	80.10±10.89	—	—	0.25–0.26	0.25±0.006	46.8–59.7	53.70±6.50	Wet weight	Burioli et al., 2017
	Marano (Italy, Lagoon)	6	Soft Tissue	55.2–107.3	72.62±19.71	0.18–0.4	0.26±0.08	10.3–16.1	13.50±3.42	94.2–126.4	104.70±12.98	—	—	0.15–0.27	0.20±0.05	62.2–184.2	228.70±297.11	Wet weight	Burioli et al., 2017
	Orbetello (Italy, Lagoon)	6	Soft Tissue	18.7–65.8	31.72±17.09	0.002–0.17	0.09±0.05	7.9–15.7	10.90±2.85	36.8–79.0	47.33±16.12	—	—	0.13–0.27	0.18±0.05	71.4–128.9	86.32±22.78	Wet weight	Burioli et al., 2017
	Capoiale-Varano (Italy, Lagoon)	9	Soft Tissue	14.6–97.1	38.92±26.10	0.052–0.22	0.11±0.05	10.7–16.7	13.9±2.25	30.3–94.2	59.09±19.38	—	—	0.13–0.23	0.17±0.04	31.8–433.2	188.71±142.45	Wet weight	Burioli et al., 2017
Perna viridis	Parangipettai (India)	—	Soft Tissue	—	42.11	—	0.86	—	13.08	—	132.25	—	0.21	—	0.46	—	11.15		Satheeswaran et al., 2019
Meretrix lusoria	Parangipettai (India)	—	Soft Tissue	—	33.35	—	0.66	—	4.75	—	60.27	—	0.39	—	0.52	—	7.81		Satheeswaran et al., 2019
Ostrea edulis	Parangipettai (India)	—	Soft Tissue	—	36.16	—	0.84	—	4.2	—	80.49	—	0.11	—	0.23	—	18.4		Satheeswaran et al., 2019
Venerupis decussata	Elluouza (Tunisia )	8 (20 per pool)	Gills	—	19.84±0.50	—	—	—	—	—	367.39±7.41	—	—	—	0.32±0.05	—	4.10±1.11		Bejaoui et al., 2020
			Digestive gland	—	16.90±4.25	—	—	—	—	—	395.92±15.03	—	—	—	0.42±0.07	—	5.39±0.97		Bejaoui et al., 2020
	Bizerte Lagoon (Tunisia)	8 (20 per pool)	Gills	—	21.47±2.88	—	—	—	—	—	369.35±6.22	—	—	—	0.44±0.03	—	4.89±0.83		Bejaoui et al., 2020
			Digestive gland	—	20.96±4.16	—	—	—	—	—	406.36±12.66	—	—	—	0.54±0.09	—	5.54±0.95		Bejaoui et al., 2020
	North Tunis Lagoon (Tunisia)	8 (20 per pool)	Gills	—	21.32±2.76	—	—	—	—	—	345.27±6.94	—	—	—	0.59±0.03	—	4.69±1.04		Bejaoui et al., 2020
			Digestive gland	—	20.25±3.98	—	—	—	—	—	402.92±8.97	—	—	—	0.58±0.12	—	6.31±0.65		Bejaoui et al., 2020
	South Tunis Lagoon (Tunisia)	8 (20 per pool)	Gills	—	23.83±1.43	—	—	—	—	—	373.74±10.97	—	—	—	0.77±0.10	—	6.87±1.02		Bejaoui et al., 2020
			Digestive gland	—	21.87±4.25	—	—	—	—	—	433.83±13.51	—	—	—	0.82±0.18	—	8.42±1.06		Bejaoui et al., 2020
	Boughrara Lagoon (Tunisia)	8 (20 per pool)	Gills	—	22.49±0.51	—	—	—	—	—	377.37±7.32	—	—	—	1.06±0.10	—	8.77±1.13		Bejaoui et al., 2020
			Digestive gland	—	22.99±4.32	—	—	—	—	—	435.22±13.07	—	—	—	0.84±0.09	—	8.13±1.17		Bejaoui et al., 2020
Patella caerulea	Sicilian Coast (Italy)		Soft Tissue	—	—	0.10–1.01	—	—	—	—	—	—	—	—	—	0.47–3.79	—		Cubadda et al., 2001
	Tyrrhenian Sea (Italy)		Soft Tissue	—	—	0.72–0.96	—	—	—	—	—	—	—	—	—	10.2–19.2	—		Conti and Cecchetti, 2003
	Lebanese Sea (Italy)		Soft Tissue	—	—	—	—	—	—	—	—	—	—	—	—	—	—		Nakhlé et al., 2006
	Iskenderun (Turkey)		Soft Tissue	—	—	—	—	—	—	61.2–213	—	0.15–0.33	—	0.53–1.60	—	1.38–5.58	—		Yüzereroğlu et al., 2010
	Yumurtalik (Turkey)		Soft Tissue	—	—	—	—	—	—	36.6–169	—	0.05–0.14	—	0.39–1.05	—	1.09–2.12	—		Yüzereroğlu et al., 2010
	Tyrrhenian Sea, Central Italy		Soft Tissue	—	—	0.46–1.31	—	—	—	—	—	—	—	—	—	5.51–11.50	—		Conti and Cecchetti, 2003
Mytilus galloprovincialis	Cala Iris Al Hoceima (Moroco)		Soft Tissue	—	—	—	—	—	—	340–673	—	N.D.	—	2.03–3.82	—	5.28–6.16	—		Azizi et al., 2018
	Izmir Bay (Turkey)		Soft Tissue	—	—	—	—	1.23–2.00	—	—	—	—	—	1.09–1.84	—	0.71–1.72	—		Kontas, 2012
Brachidontes variabillis	Lebanese Coast (Lebanon)		Soft Tissue	—	—	—	—	—	—	—	—	—	—	—	—	—	—		Nakhlé et al., 2006
Donax trunculus	Eastern Harbour (Egypt)		Soft Tissue	—	—	—	—	—	21.2±0.23	—	570±8	—	—	—	—	—	12.57±0.22		Abdallah and Abdallah, 2008
	Atlantic Coast (Southern Spain)	30	Soft Tissue	—	—	0.34–2.11	1.2	—	—	—	—	—	—	0.51–1.66	1.2	60–383	175		Usero et al., 2005
Spondylus spinosus	Lebanese coast (Lebanon)	60	Soft Tissue	0.77–85.1	11.1±13.4	0.30–0.93	0.54±0.14	0.75–14.76	4.51±2.98	6.78–136	27.6±24.5	0.27–2.36	0.86±0.46	0.86–13.9	6.47±3.27	1.06–31.03	8.50±6.45		Ghosn et al., 2020
	Iskenderun Bay (Turkey)		Soft Tissue	66.0–113	—	9.78–18.1	—	24.8–30.6	—	64.4–251	—	3.47–9.85	—	—	—	14.5–20.4	—		Türkmen and Türkmen, 2005
Tegillarca granosa	Sanmen Bay (China)	6	Soft Tissue	—	—	0.21–0.73	0.46±0.16	—	—	—	—	—	—	—	—	0.92–4.36	2.44±1.44	Wet weight	Liu et al., 2018
Sinonovacula constricta	Sanmen Bay (China)	3	Soft Tissue	—	—	0.15–0.57	0.34±0.21	—	—	—	—	—	—	—	—	1.13–4.12	2.97±1.61	Wet weight	Liu et al., 2018
Barbatia obliquata	Sanmen Bay (China)	6	Soft Tissue	—	—	0.14–0.40	0.23±0.10	—	—	—	—	—	—	—	—	1.51–3.09	2.24±0.57	Wet weight	Liu et al., 2018
Mytilus edulis	Sanmen Bay (China)	3	Soft Tissue	—	—	0.15–0.61	0.43±0.25	—	—	—	—	—	—	—	—	2.36–5.38	4.11±1.57	Wet weight	Liu et al., 2018
Mactra ovalina	Kunduchi (Tanzania)	3	Soft Tissue	—	251	—	0.68	—	39	—	455	—	0.5	—	2	—	14		Rumisha et al., 2012
	Msa sani (Tanzania)	3	Soft Tissue	—	1,307	—	4.98	—	20	—	1,425	—	0.9	—	5	—	15		Rumisha et al., 2012
	Msimbazi (Tanzania)	3	Soft Tissue	—	166	—	1.9	—	428	—	316	—	2.1	—	2.7	—	22		Rumisha et al., 2012
Chamelea gallina	Atlantic Coast (Southern Spain)	30	Soft Tissue	—	—	0.24–1.22	0.70	—	—	—	—	—	—	1.41–2.23	1.9	9.2–90	38		Usero et al., 2005

Sample name	site	n	Organ	Zn		As		Se		Cd		Tl		Pb		Note	Referrence
				Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD
This Study
Cyclina sinensis	Haneda (Esutuary of Tama River)	6	Muscle	164–292	210±41	4.52–7.08	5.67±0.88	9.22–12.5	10.6±1.1	<0.00008–0.0740	0.0740	<0.005	<0.005	<0.005	<0.005		—
			Others	98.6–148	121±16	6.77–10.1	8.46±1.04	9.96–15.2	13.2±1.6	0.0956–0.191	0.135±0.040	<0.005	<0.005	0.764–1.27	0.951±0.196		—
Crassostrea gigas	Haneda (Esutuary of Tama River)	6	Muscle	1,700–5.050	3,140±1,080	5.59–9.61	7.56±1.12	3.52–7.15	5.52±1.03	1.70–2.78	2.15±0.41	<0.005	<0.005	0.914–1.64	1.28±0.30		—
			Others	1,480–2,620	2,020±376	6.37–13.4	11.0±2.3	3.21–7.90	6.50±1.57	0.777–2.44	1.53±0.56	<0.005	<0.005	0.798–1.50	1.19±0.27		—
Mactra veneriformis	Haneda (Esutuary of Tama River)	7	Muscle	116–194	138±33	3.03–5.81	4.32±0.83	6.21–56.9	28.9±21.8	<0.00008–0.155	0.147	<0.005	<0.005	<0.005–0.444	0.434		—
			Others	114–238	184±49	2.31–6.87	4.88±1.48	3.27–11.2	5.51±2.88	0.211–0.316	0.261±0.043	<0.005	<0.005	2.09–4.42	2.98±0.89		—
Mactra veneriformis	Kasai (Tokyo Sea Life Park)	5	Muscle	102–133	133±102	4.70–10.3	6.50±1.97	1.65–3.23	2.53±0.56	0.209–0.540	0.341±0.117	0.0110–0.0153	0.0135±0.0018	0.421–3.15	1.28±1.10		—
			Others	114–161	131±17	8.72–12.3	10.3±1.3	3.38–5.45	4.40±0.77	0.330–1.05	0.513±0.270	0.0106–0.0320	0.0181±0.0077	0.753–5.57	1.86±1.86		—
Previous Research
Crassostrea gigas	La Pitahaya channel (Mexico)	20	Soft Tissue	95.10–416.67	278.91±93.03	0.07–0.42	0.58±0.91	—	—	4.07–21.33	14.54±4.28	—	—	<LDM–4.67	2.22±1.33		Jonathan et al., 2017
	Caorle (Italy, Open Sea)	6	Soft Tissue	168.3–335.4	246.90±65.23	2.4–4.3	3.30±0.87	0.56–1.1	0.86±0.21	0.58–0.71	0.65±0.06	<0.010	<0.010	0.16–0.20	0.18±0.02	Wet weight	Burioli et al., 2017
	Cervia (Italy, Open Sea)	6	Soft Tissue	240.1–513.2	381.83±141.82	2.4–8.2	3.75±2.20	0.01–0.72	0.58±0.47	0.39–0.64	0.51±0.09	<0.010	<0.010	0.12–0.22	0.17±0.04	Wet weight	Burioli et al., 2017
	Monfalcone (Italy, Gulf)	3	Soft Tissue	472.8–630.1	552.97±78.69	2.3–3.4	2.73±0.59	0.89–1.1	0.99±0.11	0.61–0.71	0.67±0.05	<0.010	<0.010	0.14–0.2	0.17±0.03	Wet weight	Burioli et al., 2017
	Muggia (Italy, Gulf)	3	Soft Tissue	776.4–1,142.2	908.87±202.69	9.0–15.5	11.33±3.62	—	1.30	0.51–0.76	0.61±0.13	<0.010	<0.010	0.66–0.76	0.72±0.05	Wet weight	Burioli et al., 2017
	Giulianova (Italy, Gulf)	6	Soft Tissue	479.8–767.2	675.78±106.37	4.4–7.4	5.32±1.08	0.8–1.2	1.01±0.13	0.17–0.41	0.26±0.09	<0.010	<0.010	0.27–0.44	0.33±0.07	Wet weight	Burioli et al., 2017
	Porto Garibaldi (Italy, Harbor)	3	Soft Tissue	339.8–635.9	444.77±165.79	2.4–3.3	2.93±0.47	0.81–1.1	0.88±0.10	0.29–0.33	0.32±0.02	<0.010	<0.010	0.11–0.15	0.14±0.02	Wet weight	Burioli et al., 2017
	Caleri (Italy, Lagoon)	9	Soft Tissue	14.8–286.1	156.84±77.85	3.1–6.6	4.85±1.11	0.68–0.98	0.78±0.10	0.16–0.37	0.24±0.06	<0.010	<0.010	0.16–0.28	0.22±0.04	Wet weight	Burioli et al., 2017
	Cavallino-Trepoti (Italy. Lagoon)	12	Soft Tissue	573.6–1,970.6	1,090.69±387.20	1.4–4.0	2.64±0.92	0.46–0.82	0.63±0.12	0.065–0.21	0.13±0.05	<0.010	<0.010	0.086–0.44	0.22±0.11	Wet weight	Burioli et al., 2017
	Chioggia (Italy, Lagoon)	3	Soft Tissue	338.1–528.7	452.10±100.65	2.9–3.6	3.33±0.38	0.86–1.0	0.92±0.074	0.17–0.2	0.18±0.02	<0.010	<0.010	0.2–0.21	0.20±0.006	Wet weight	Burioli et al., 2017
	Marano (Italy, Lagoon)	6	Soft Tissue	219.4–626.1	421.33±152.66	2.1–3.1	2.53±0.40	0.94–1.4	1.14±0.18	0.12–0.15	0.13±0.01	<0.010	<0.010	0.17–0.24	0.20±0.02	Wet weight	Burioli et al., 2017
	Orbetello (Italy, Lagoon)	6	Soft Tissue	190.0–486.0	260.92±113.22	6.1–8.0	7.22±0.79	0.6–0.95	0.80±0.14	0.085–0.14	0.11±0.02	<0.010	<0.010	0.16–0.22	0.18±0.02	Wet weight	Burioli et al., 2017
	Capoiale-Varano (Italy, Lagoon)	9	Soft Tissue	143.1–559.4	281.06±141.40	2.2–8.8	5.28±2.20	1.0–1.3	1.16±0.10	0.47–1.1	0.68±0.23	<0.010	<0.010	0.075–0.31	0.20±0.08	Wet weight	Burioli et al., 2017
Perna viridis	Parangipettai (India)	—	Soft Tissue	—	19	—	—	—	—	—	0.86	—	—	—	0.94		Satheeswaran et al., 2019
Meretrix lusoria	Parangipettai (India)	—	Soft Tissue	—	37.79	—	—	—	—	—	0.66	—	—	—	2.45		Satheeswaran et al., 2019
Ostrea edulis	Parangipettai (India)	—	Soft Tissue	—	75.62	—	—	—	—	—	0.84	—	—	—	0.53		Satheeswaran et al., 2019
Venerupis decussata	Elluouza (Tunisia )	8 (20 per pool)	Gills	—	25.73±5.35	—	—	—	—	—	0.85±0.09	—	—	—	0.99±0.17		Bejaoui et al., 2020
			Digestive gland	—	36.08±15.03	—	—	—	—	—	0.87±0.10	—	—	—	1.13±0.33		Bejaoui et al., 2020
	Bizerte Lagoon (Tunisia)	8 (20 per pool)	Gills	—	30.51±2.52	—	—	—	—	—	0.92±0.12	—	—	—	1.29±0.10		Bejaoui et al., 2020
			Digestive gland	—	36.52±7.02	—	—	—	—	—	1.03±0.10	—	—	—	1.66±0.46		Bejaoui et al., 2020
	North Tunis Lagoon (Tunisia)	8 (20 per pool)	Gills	—	30.83±3.95	—	—	—	—	—	0.90±0.18	—	—	—	1.38±0.27		Bejaoui et al., 2020
			Digestive gland	—	37.17±7.33	—	—	—	—	—	1.01±0.07	—	—	—	1.82±0.31		Bejaoui et al., 2020
	South Tunis Lagoon (Tunisia)	8 (20 per pool)	Gills	—	32.02±6.88	—	—	—	—	—	1.26±0.18	—	—	—	1.68±0.17		Bejaoui et al., 2020
			Digestive gland	—	50.44±6.36	—	—	—	—	—	1.32±0.10	—	—	—	2.33±0.31		Bejaoui et al., 2020
	Boughrara Lagoon (Tunisia)	8 (20 per pool)	Gills	—	34.19±6.95	—	—	—	—	—	1.42±0.25	—	—	—	1.91±0.21		Bejaoui et al., 2020
			Digestive gland	—	50.08±6.23	—	—	—	—	—	1.87±0.38	—	—	—	2.31±0.32		Bejaoui et al., 2020
Patella caerulea	Sicilian Coast (Italy)		Soft Tissue	2.2–19.1	—	—	—	—	—	1.7–11.8	—	—	—	0.06–2.18	—		Cubadda et al., 2001
	Tyrrhenian Sea (Italy)		Soft Tissue	—	—	—	—	—	—	2.89–4.06	—	—	—	0.51–1.50	—		Conti and Cecchetti, 2003
	Lebanese Sea (Italy)		Soft Tissue	—	—	—	—	—	—	0.6–8.7	—	—	—	0.50–2.60	—		Nakhlé et al., 2006
	Iskenderun (Turkey)		Soft Tissue	6.50–13.71	—	—	—	—	—	0.41–0.68	—	—	—	0.13–0.70	—		Yüzereroğlu et al., 2010
	Yumurtalik (Turkey)		Soft Tissue	3.70–9.84	—	—	—	—	—	0.24–0.44	—	—	—	0.05–0.31	—		Yüzereroğlu et al., 2010
	Tyrrhenian Sea, Central Italy		Soft Tissue	—	—	—	—	—	—	0.32–0.49	—	—	—	1.67–2.49	—		Conti and Cecchetti, 2003
Mytilus galloprovincialis	Cala Iris Al Hoceima (Moroco)		Soft Tissue	160–164	—	—	—	—	—	0.65–0.85	—	—	—	N.D.	—		Azizi et al., 2018
	Izmir Bay (Turkey)		Soft Tissue	18.7–30.0	—	—	—	—	—	—	—	—	—	—	—		Kontas, 2012
Brachidontes variabillis	Lebanese Coast (Lebanon)		Soft Tissue	—	—	—	—	—	—	1.08–4.0	—	—	—	1.0–2.5	—		Nakhlé et al., 2006
Donax trunculus	Eastern Harbour (Egypt)		Soft Tissue	—	74.0±4.5	—	—	—	—	—	3.93±0.20	—	—	—	—		Abdallah and Abdallah, 2008
	Atlantic Coast (Southern Spain)	30	Soft Tissue	56–152	107	4.9–12.1	8.5	—	—	0.15–0.24	0.19	—	—	1.1–9.5	3.6		Usero et al., 2005
Spondylus spinosus	Lebanese coast (Lebanon)	60	Soft Tissue	42.9–972	124±162	9.52–186	35.2±27.4	1.42–5.25	3.00±0.94	0.54–7.74	3.00±1.33	—	—	0.12–3.54	0.89±0.87		Ghosn et al., 2020
	Iskenderun Bay (Turkey)		Soft Tissue	64.8–82.8	—	—	—	—	—	4.96–15.1	—	—	—	59.9–132	—		Türkmen and Türkmen, 2005
Tegillarca granosa	Sanmen Bay (China)	6	Soft Tissue	12.11–18.51	15.66±2.44	1.42–4.20	2.81±1.35	—	—	0.22–1.92	1.09±0.64	—	—	0.09–0.37	0.21±0.10	Wet weight	Liu et al., 2018
Sinonovacula constricta	Sanmen Bay (China)	3	Soft Tissue	16.37–31.74	24.17±7.69	1.96–2.85	2.36±0.45	—	—	0.18–0.20	0.19±0.01	—	—	0.18–0.47	0.28±0.16	Wet weight	Liu et al., 2018
Barbatia obliquata	Sanmen Bay (China)	6	Soft Tissue	14.22–20.78	16.67±2.84	2.93–6.88	5.27±1.52	—	—	0.65–1.76	1.08±0.42	—	—	0.17–0.35	0.23±0.07	Wet weight	Liu et al., 2018
Mytilus edulis	Sanmen Bay (China)	3	Soft Tissue	14.58–24.98	21.00±5.61	2.18–2.83	2.61±0.37	—	—	0.52–0.66	0.59±0.07	—	—	0.03–0.14	0.10±0.06	Wet weight	Liu et al., 2018
Mactra ovalina	Kunduchi (Tanzania)	3	Soft Tissue	—	201	—	2.6	—	—	—	0.2	—	0.008	—	6.2		Rumisha et al., 2012
	Msa sani (Tanzania)	3	Soft Tissue	—	65	—	6.0	—	—	—	0.1	—	0.051	—	4.2		Rumisha et al., 2012
	Msimbazi (Tanzania)	3	Soft Tissue	—	163	—	0.7	—	—	—	0.2	—	0.004	—	4.4		Rumisha et al., 2012
Chamelea gallina	Atlantic Coast (Southern Spain)	30	Soft Tissue	61–92	72	5.3–8.3	6.4	—	—	0.29–0.38	0.33	—	—	0.74–1.92	1.3		Usero et al., 2005

N.D.: Not detected.

Table 5 Comparison of trace element concentrations (μg/g) in crustaceans, using results of this study and previous studies

Sample name	site	n	Organ	Al		V		Cr		Mn		Fe		Co		Note	Referrence
				Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD
This study
Hemigrapsus penicillatus	Haneda (Estuary of Tama River)	5	Muscle	25.2–130	66.8±41.6	0.177–0.309	0.263±0.061	<0.001	<0.001	11.3–105	60.2±32.1	50.8–324	198±96	0.309–0.466	0.377±0.066		—
			Hepatopancreas	715–8,630	4,130±2,730	1.87–18.8	9.73±5.87	1.34–11.6	7.34±4.08	55.7–388	215±110	1,240–12,500	6,370±3,860	1.61–7.27	3.93±1.90		—
Macrophthalmus japonicus	Haneda (Estuary of Tama River)	5	Muscle	194–572	380±122	0.578–1.45	0.937±0.307	0.851–1.28	1.08±0.18	23.0–191	82.9±60.2	391–883	579±166	0.186–0.768	0.399±0.213		—
			Hepatopancreas	133–4,650	2,060±1,740	0.875–10.0	4.88±3.43	0.313–7.84	4.36±2.69	228–367	310±59	277–6,580	3,030±2,410	0.33–3.40	1.71±1.07		—
Pyrhila pisum	Haneda (Estuary of Tama River)	5	Hepatopancreas	19.4–1,230	393±433	0.956–3.08	1.64±0.84	<0.001–1.35	1.01	21.5–68.2	43.4±18.0	166–1,880	810±582	1.15–1.90	1.64±0.30		—
Macrophthalmus japonicus	Kasai (Tokyo Sea Life Park)	3	Hepatopancreas	2,070–9,280	5,850±2,950	3.38–14.5	8.85±4.54	2.55–12.0	7.55±3.88	232–442	315±91	1,850–8,040	5,210±2,550	1.11–3.78	2.74±1.17		—
Previous Research
Portunus trituberculatus	Sanmen Bay (China)	7	Soft Tissue	—	—	—	—	0.06–0.44	0.15±0.13	—	—	—	—	—	—	Wet weight	Liu et al., 2018
Portunus pelagicus	South East Coast of India	42	Gill	—	—	—	—	BDL	—	BDL–60.88	13.13	—	—	BDL–1.55	0.45		Kumar et al., 2019
			Muscle	—	—	—	—	BDL–81.69	2.90	BDL–16.84	2.90	—	—	BDL–0.62	0.08		Kumar et al., 2019
			Hepatopancreas	—	—	—	—	BDL	—	BDL–225.63	42.43	—	—	BDL–1.66	0.46		Kumar et al., 2019
Portunus sanguinolentus	South East Coast of India	48	Gill	—	—	—	—	BDL	BDL	BDL–53.74	14.85	—	—	BDL–3.84	0.66		Kumar et al., 2019
			Muscle	—	—	—	—	BDL–163.23	16.31	BDL–56.15	6.09	—	—	BDL–6.32	0.36		Kumar et al., 2019
			Hepatopancreas	—	—	—	—	BDL	BDL	BDL–159.76	19.47	—	—	BDL–2.58	0.37		Kumar et al., 2019
Pachygrapsus marmoratus	Tuscany Coast (Italy)	13	Soft Tissue	—	—	—	—	—	5.40±5.95	—	—	—	—	—	—	Wet weight	Bonsignore et al., 2018
Dotilla fenestrata	Durban Harbour (South Africa)		Gill	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Exosleleton	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Digestive Gland	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
	Richards Bay Harbour (South Africa)		Gill	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Exosleleton	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Digestive Gland	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
	Mulalazi Estuary (South Africa)		Gill	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Exosleleton	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020
			Digestive Gland	—	—	—	—	—	—	—	—	—	—	—	—		Adeleke et al., 2020

Sample name	site	n	Organ	Ni		Cu		Zn		As		Se		Cd		Tl		Pb		Note	Referrence
				Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD	Range	Average±SD
This study
Hemigrapsus penicillatus	Haneda (Estuary of Tama River)	5	Muscle	0.746–8.86	3.18±2.94	99.7–131	111±11	175–454	247±105	4.52–10.5	7.44±2.19	1.62–3.68	2.22±0.77	<0.00008	<0.00008	<0.005	<0.005	<0.005–0.721	0.721		—
			Hepatopancreas	4.81–18.6	11.3±4.8	203–382	311±68	124–203	160±30	4.98–7.57	6.36±0.89	3.58–8.27	5.27±1.68	0.357–0.685	0.536±0.116	<0.005	<0.005	1.16–9.42	5.54±2.95		—
Macrophthalmus japonicus	Haneda (Estuary of Tama River)	5	Muscle	0.651–2.00	1.51±0.48	84.3–116	104±11	220–296	252±25	1.48–2.91	2.40±0.51	3.08–3.49	3.30±0.15	<0.00008	<0.00008	<0.005	<0.005	0.472–1.06	0.719±0.214		—
			Hepatopancreas	0.730–6.81	3.69±2.12	153–604	379±186	123–244	180±52	3.98–8.55	6.28±1.89	4.93–6.70	6.13±0.64	0.214–1.42	0.832±0.486	<0.005	<0.005	0.503–5.97	2.91±2.12		—
Pyrhila pisum	Haneda (Estuary of Tama River)	5	Hepatopancreas	1.54–3.60	2.51±0.74	36.9–78.5	53.0±14.2	132–214	167±30	5.52–10.1	7.09±1.57	4.51–7.52	6.32±1.09	0.210–1.19	0.673±0.312	<0.005	<0.005	0.682–2.18	1.49±0.68		—
Macrophthalmus japonicus	Kasai (Tokyo Sea Life Park)	3	Hepatopancreas	3.34–11.2	7.48±3.22	203–288	254±37	126–175	144±22	7.34–8.92	8.13±0.65	4.51–6.43	5.69±0.84	0.452–0.568	0.505±0.048	<0.005	<0.005	1.54–6.25	4.52±2.11		—
Previous Research
Portunus trituberculatus	Sanmen Bay (China)	7	Soft Tissue	—	—	2.14–4.74	3.56±0.93	31.37–59.31	44.14±10.19	5.67–7.19	6.62±0.60	—	—	0.01–0.10	0.03±0.03	—	—	N.D.-0.20	0.04±0.07	Wet weight	Liu et al., 2018
Portunus pelagicus	South East Coast of India	42	Gill	0.86–6.09	2.01	58.25–267.26	134.31	—	—	—	—	—	—	BDL–6.50	2.20	—	—	BDL–8.68	1.26		Kumar et al., 2019
			Muscle	BDL–32.77	6.79	BDL–156.84	28.59	—	—	—	—	—	—	BDL–2.74	0.72	—	—	BDL–1.37	0.13		Kumar et al., 2019
			Hepatopancreas	BDL–14.86	3.62	BDL–222.92	62.93	—	—	—	—	—	—	BDL–30.23	6.83	—	—	BDL–4.32	0.46		Kumar et al., 2019
Portunus sanguinolentus	South East Coast of India	48	Gill	0.93–7.33	2.15	43.52–259.43	133.94	—	—	—	—	—	—	BDL–15.78	2.95	—	—	BDL–6.50	1.32		Kumar et al., 2019
			Muscle	0.01–86.41	12.84	BDL–59.11	71.93	—	—	—	—	—	—	BDL–4.08	1.22	—	—	BDL–2.10	0.22		Kumar et al., 2019
			Hepatopancreas	BDL–34.35	4.45	BDL–375.94	14.21	—	—	—	—	—	—	BDL–46.47	10.31	—	—	BDL–2.57	0.36		Kumar et al., 2019
Pachygrapsus marmoratus	Tuscany Coast (Italy)	13	Soft Tissue	—	6.63±7.45	—	43.7±7.59	—	58.5±52.4	—	9.51±5.40	—	—	—	0.06±0.02	—	—	—	3.56±2.81	Wet weight	Bonsignore et al., 2018
Dotilla fenestrata	Durban Harbour (South Africa)		Gill	—	—	78.5±3.30		—	27.6±3.72	—	—	—	—	—	0.27±0.00	—	—	—	3.17±0.30		Adeleke et al., 2020
			Exosleleton	—	—	83.8±1.56		—	26.4±0.32	—	—	—	—	—	0.42±0.00	—	—	—	2.43±0.10		Adeleke et al., 2020
			Digestive Gland	—	—	63.7±1.01		—	19.4±0.57	—	—	—	—	—	0.41±0.02	—	—	—	4.71±0.20		Adeleke et al., 2020
	Richards Bay Harbour (South Africa)		Gill	—	—	52.5±4.86		—	13.4±1.40	—	—	—	—	—	0.15±0.00	—	—	—	1.54±0.10		Adeleke et al., 2020
			Exosleleton	—	—	27.7±1.07		—	9.54±0.35	—	—	—	—	—	0.22±0.02	—	—	—	1.23±0.13		Adeleke et al., 2020
			Digestive Gland	—	—	20.4±0.14		—	6.78±0.16	—	—	—	—	—	0.13±0.03	—	—	—	1.58±0.10		Adeleke et al., 2020
	Mulalazi Estuary (South Africa)		Gill	—	—	23.8±1.09		—	6.71±0.64	—	—	—	—	—	0.18±0.03	—	—	—	1.68±0.03		Adeleke et al., 2020
			Exosleleton	—	—	18.7±0.26		—	6.91±0.12	—	—	—	—	—	0.17±0.02	—	—	—	3.53±0.27		Adeleke et al., 2020
			Digestive Gland	—	—	15.0±0.17		—	4.69±0.11	—	—	—	—	—	0.18±0.00	—	—	—	1.72±0.23		Adeleke et al., 2020

BDL: Below detection limit. N.D.: Not detected.

Analysis of trace element concentrations in invertebrates at Kasai showed that most elements detected in each tissue of a species at Haneda were similar at Kasai (Tables 2 and 3). Most high-toxicity element concentrations in M. veneriformis at Kasai were similar to those in Haneda except for Cr and Cu (Table 4). However, Mn, Co, As and Cd concentrations in M. veneriformis were higher at Kasai than at Haneda. Aluminum, V, Cr, Mn, Fe, Co, Ni, As, and Pb concentrations in M. japonicus at Kasai were higher than in Haneda (Table 5). Zinc was detected at similar levels in invertebrates in Haneda and Kasai. Thus, invertebrates in Kasai were likely exposed to similar or higher levels of high-toxicity elements than in Haneda. Furthermore, Tl was detected from M. veneriformis in Kasai; however, the concentration was lower than that in M. ovalina in a heavily polluted area in Tanzania, but similar to levels in other polluted areas (Rumisha et al., 2012). A Tl influx in Kasai and occurrence of pollution in bivalves living in sediment were shown. Thallium is also highly toxic, and its lethal concentration in humans is 10–15 mg/kg (Munch, 1934; Moore et al., 1993). Thallium ions are reported to accumulate in larvae of the nematode Caenorhabditis elegans and result in decreased survival, delayed growth, abnormal behavior, and oxidative stress (Varão et al., 2021). A similar effect may occur in M. veneriformis in Kasai. Although the amount of contamination is currently very small, if this continues in the future, the risk of health hazards due to human ingestion of M. veneriformis in Kasai and bioaccumulation in higher trophic-level organisms is possible. Figs. 3, 4, 5 show the results of PCA using trace element concentrations in each tissue of M. veneriformis and hepatopancreas of M. japonicus in Haneda and Kasai. In M. veneriformis, individuals at each site were divided by PC1. This tendency was indicated in both tissues. There were differences in element composition between the two sites. Differences in rivers flowing into the collection site are suggested: Haneda has the Tamagawa River, but Kasai has the Kyuedokawa and Arakawa Rivers. Some essential elements were characteristic in muscles in M. veneriformis in Haneda: Mg, K, Ca, Cr and Ni (Fig. 3). Most elements, including highly toxic Co, As and Cd were characteristic in M. veneriformis muscles in Kasai; these same elements were also characteristic in M. veneriformis internal organs in Kasai (Fig. 4). Since most of the high toxicity elements were characterized in Kasai, the statistical analysis indicated that contamination by high-toxicity elements in M. veneriformis in Kasai was more serious than in Haneda. Furthermore, Zn was not characteristic in either site (Figs. 3 and 4). The statistical analysis supported the existence of common strong Zn contamination in both sites. Individuals from each site of M. japonicus were dispersed with no clear difference between sites (Fig. 5); however, most elements were found in a single M. japonicus individual in Kasai. The different element concentrations among individuals of the same species were also considered in the comparison between sites. Therefore, bivalves may be superior to crustaceans when comparing the element distributions among different areas because differences among individuals are less likely.

Fig. 3

Result of principal component analysis using the element concentrations in muscle of Mactra veneriformis collected from Haneda and Kasai in June and July 2019, respectively

Fig. 4

Result of principal component analysis using the element concentrations in internal organs of Mactra veneriformis collected from Haneda and Kasai in June and July 2019, respectively

Fig. 5

Result of principal component analysis using the element concentrations in internal organs of Macrophthalmus japonicus collected from Haneda and Kasai in June and July 2019, respectively

Contamination by highly toxic elements exists in Haneda and Kasai. The sampling sites of Kasai are well managed, with less waste than in Haneda. But the levels of trace elements contamination in Kasai was similar to Haneda. Therefore, inflow from upstream is considered to be the main cause of contamination in Kasai. It is assumed that more element species flow into Kasai in terms of both species and quantity than in Haneda.

CONCLUSION

Hypoxia tolerance may affect element distribution both within tissues and between species in bivalves. However, few studies have examined the relationship between hypoxia tolerance and trace elements. The combined effects of hypoxia and trace elements should be assessed in various bivalve species and clarified. Additionally, differences in distribution of elements by bivalve habitat were indicated. More accurate marine monitoring should use several bivalve species with different habitats. In contrast, distribution of trace elements in crustaceans was affected by their food type. Additionally, element contamination was higher in detritus-feeding species than carnivores. Especially, the effect of MP was stronger in detritus-eating crustaceans than in carnivores and bivalves. Detritus-eating crustaceans are effective for environmental monitoring of MP. However, it should be noted that the distribution of elements among crustacean species was not as clear as for bivalves.

In Haneda, Al and Zn contaminations were more serious than in other polluted areas. Some elements’, except Al and Zn, concentrations were also at similar levels to those in other polluted areas. Moreover, invertebrates in Kasai showed the same concentration levels as in Haneda. But some differences are indicated of element species to inflow in Kasai and Haneda, especially highly toxic Tl. Contamination by several highly toxic elements is continuing in Tokyo Bay and continuous monitoring in a wide area of the deep part of Tokyo Bay is necessary.

ACKNOWLEDGMENTS

We thank Otaku Kankyo Meisters. This study was supported by The University of Tokyo FSI—Nippon Foundation Research Project on Marine Plastics.

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