Bioaccumulation of some trace elements

Boletínindethe biota of hydrothermal fields of the Guaymas Basin (Gulf of California)

la Sociedad Geológica Mexicana
31

Volumen 61, núm. 1, 2009, p. 31-45 D GEOL

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Bioaccumulation of some trace elements in the biota of hydrothermal

fields of the Guaymas Basin (Gulf of California)
Ludmila L. Demina1,*, Sergey V. Galkin1 and Evgueni N. Shumilin2
1
P.P.Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia
2
Centro Interdisciplinario de Ciencias Marinas, Avenida IPN s/n, Col. Playa Palo de Santa Rita, Apartado Postal 592, La Paz, Baja
California Sur, 23096, Mexico
*
[email protected]

Abstract

Data from the hydrothermally influenced Guaymas Basin of the Gulf of California are presented on the concentration and distribution
of Ag, As, Au, Ba, Cd, Co, Cr, Cu, Fe, Hg, Mn, Pb, Sb, Se, and Zn in different tissues of dominant hydrothermal vent animals such as
vestimentifera Riftia pachyptila and vesicomyid clams Archivesica gigas and other organisms, including Spongia, bivalve mollusks
Nuculana grasslei, Phelliactis pabista, and crab Munidopsis alvisca. Chemical element content was measured by atomic absorption
spectrometry (flame and graphite furnace methods) and instrumental neutron activation analysis.
In the dominant specialized taxa, the main target organs of metals were the trophosome and obturaculae of Riftia pachyptila, the
gills and mantle of Archivesica gigas. The other organisms also demonstrated high bioaccumulation of metals. Especially high levels of
most of the metals (excluding Mn) were detected in the soft body of Nuculana grasslei. The highest Mn content was found in the whole
body of Spongia. Bioconcentration factor of the trace metals studied varies within three orders of magnitude from 5 (Mn) to 3•104 (Cd).
This testifies apparently a selectivity of trace metal bioaccumulation by the organisms which is determined by metal bioavailability
independently of metal concentration in the water column. Variability in the molar ratio Fe/Mn allows us to assume that these metals
undergo fractionation during migration from the hydrothermal fluids to the interior organs of animals. Insignificant differences between
the Cd, Cu, Fe, Hg, Pb, and Zn levels in the Guaymas Basin vent clams versus that in the bivalve mollusks from polluted areas of the
Gulf of California might suggest that the metal bioavailability play an important role in the bioaccumulation.

Key words: trace metals; bioaccumulation; Guaymas Basin; hydrothermal communities.

Resumen

Se presentan los datos sobre la concentración y distribución de Ag, As, Au, Ba, Cd, Co, Cr, Cu, Fe, Hg, Mn, Pb, Sb, Se, and Zn en
diferentes tejidos de los animales predominantes en las ventilas hidrotermales tales como la vestimentifera Riftia pachyptila, la almeja
vesicomyidae Archivesica gigas, así como otros organismos, que incluyen Spongia, moluscos bivalvos Nuculana grasslei, Phelliactis
pabista, y el cangrejo Munidopsis alvisca. El contenido de los elementos químicos fue medido por medio de espectrofotometría de
absorción atómica (métodos de flama y de horno de grafito) y por el análisis instrumental de la activación neutrónica.
En la taxa especializada dominante, los órganos principales en los cuales se acumularon los metales fueron el trofosoma y
el obturaculae de Riftia pachyptila, las branquias y el manto de Archivesica gigas. Los otros organismos también mostraron alta
bioacumulación de metales. Especialmente altos niveles de la mayoría de los metales (excepto Mn) fueron detectados en el cuerpo suave
de Nuculana grassley. El contenido más alto de Mn fue encontrado en todo el cuerpo de Spongia. El factor de bioconcentración para los
metales traza estudiados varía en tres ordenes de magnitud desde 5 (Mn) a 3•104 (Cd). Esto aparentemente evidencia cierta selectividad
en la bioacumulación de los metales traza por los organismos, la cual es determinada por la biodisponibilidad independientemente
de la concentración de metales en la columna del agua. La variabilidad de la razón molar de Fe/Mn nos permite asumir que estos
32 Demina et al.

metales durante la migración desde los fluidos hidrotermales hacia los órganos internos de animales están sujetos a fraccionación.
Las diferencias insignificantes entre los niveles de Cd, Cu, Fe, Hg, Pb y Zn en las almejas de las ventilas de la Cuenca de Guaymas
y los niveles de los moluscos bivalvos de áreas contaminadas del Golfo California podrían sugerir que la biodisponibilidad de los
metales juega un papel importante en la bioacumulación.

Palabras clave: metales pesados; bioacumulación; Cuenca Guaymas; comunidades hidrotermales.

1. Introduction distribution of 15 chemical elements (including Ag, As,

Sb and Au, as well as organic carbon or Corg, for which
Deep-sea hydrothermal vent fields are inhabited by there were no published data on these organisms) in the
many thermophilic organisms that are able to survive under fauna microhabitats, the tissues and whole bodies of
extreme physical and chemical conditions, including high the hydrothermal organisms from the Guaymas Basin,
loads of trace metals and redox gases (Anonymous, 1995; including the dominant specialized symbiotrophic and the
Sarradin et al., 2008; Van Dover, 2000). An exceptional peripheric taxa. Besides, it is interesting to estimate the
feature of the semi-enclosed Guaymas Basin (Gulf of concentration factors of metals in organisms relative to the
California) hydrothermal vent field is the thick organic-rich water column. There are a some mining complexes located
sedimentary cover on the seafloor. This cover is a result of in the Baja California peninsula, as well as other different
high sedimentation rates due to Colorado River sediment types of industrial and urban activities along the coastal
input directly before dam construction or tidal resuspension zone of the Gulf of California, which sometimes could
of previously supplied terrigenous sediments in the Upper produce a deficiency of oxygen, acidic conditions and high
Gulf of California (Calvert, 1966; Carriquiry and Sánchez, discharges of heavy metals into the ecosystems. We aim to
1999; Carriquiry et al., 2001) and biogenic particles from determine whether there are any differences in the heavy
the highly productive euphotic zone (Lonsdale et al., metal content of the organisms exposed to hydrothermal
1980; De la Lanza-Espino and Soto, 1999; Thunell, 1998). and anthropogenic impacts.
High-temperature fluids are discharged to the surrounding
seawater through the vents and by ascending through the
overlying sediments, which are rich in Mn. This leads to the 2. Materials and methods
enrichment of fluids for Mn relative to Fe (Von Damm et al.,
1985), which is a characteristic feature of Guaymas Basin 2.1. Geological setting and faunal distribution
fluids compared to other vent fields. From this standpoint, it
is interesting to examine the trace metal and other element The Southern trough of the Guaymas Basin’s
contents of the hydrothermal organisms inhabiting the vent hydrothermal field is located at 2020 m depth (27°00.70’ N,
environments, especially since the relationships between 111°24.40’ W), presented in Figure 1. The intense tectonic
organisms from the Guaymas Basin and metals have not activity in this area is caused by the displacement of the
been thoroughly studied thus far. There are few articles Baja California peninsula towards the NW at a spreading
devoted to the chemical composition of Guaymas Basin rate of about 6 cm per year (Klitgord et al., 1974; Lonsdale
organisms, and those that do exist focus on heavy metals et al., 1980). An exceptional feature of the semi-enclosed
in dominant taxa inhabiting vent environment, such as Guaymas Basin’s hydrothermal vent field is the thick
vestimentifera Riftia (Lein et al., 1989; Lukashin et al., organic-rich sedimentary cover of the seafloor. This is a
1990; Ruelas-Inzunza et al., 2005), bivalve mollusks result of high sedimentation rates (1-2 mm per year) due
Archivesica gigas (Lein et al., 1989; Lukashin et al., to significant terrigenous input from the Colorado River
1990) and Vesicomya gigas (Ruelas-Inzunza et al., 2003). (Calvert, 1966) before its complete damming in 1956, tidal
Meanwhile, little is known about metal bioaccumulation resuspension of sediments from the Colorado River delta
in other taxa that live in the vent areas and their periphery in the Upper Gulf of California, and the high productivity
but are not dependent upon symbiotrophy. The dominant of the euphotic zone of the Gulf of California (De la
hydrothermal fauna studied here is represented by the Lanza-Espino and Soto, 1999; Thunell, 1998). The surface
highly specialized taxa vestimentifera Riftia pachyptila sediments of the Guaymas Basin also have a Mn-oxide-rich
and clam Vesicomyidae Archivesica gigas, both of which and (relatively) Fe-oxide-rich turbidite layer that affects the
are nutritionally dependent on the chemosynthetic bacterial distribution of C, Fe, Mn, S and some trace metals (Otero
community. We also consider other organisms such as et al., 2003). Iron is mainly pyritized in the sediments,
Spongia, bivalve mollusk Nuculana grasslei, Phelliactis while Mn is found predominantly in carbonates (41±12
pabista, and crab Munidopsis alvisca. %) and is associated with pyrite to a much lesser degree;
The aim of this work was to study features of the Co, Cr, Cu, Ni and Zn were highly pyritized (> 80 %) in
 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 33

Figure 1. Study area and location of sampling sites in the Guaymas Basin´s hydrothermal field of the Gulf of California

the sediments of the Guaymas Basin (Otero et al., 2003). Of the variety of factors determining fauna distribution,
The low-temperature hydrothermal mineral associations temperature and substratum characteristics are the easiest
on the floor of the Guaymas Basin are represented by opal to estimate during bottom observation. Precise data is
and barite, while pyrrhotite, sphalerite and chalcopyrite lacking in most cases, but numerous visual observations
are the dominant ore minerals in high-temperature areas accompanied by temperature estimations have found
(Bogdanov et al., 2004). It is interesting to note that both that black smokers have a temperature in the range 275-
mineral formations contain oil hydrocarbons, with a content 400°C, while white smoker temperature varies from 100
of C org in the surface sediments ranging from 0.15 % to 250°C (BRIDGE Workshop Report, 1994). The heat
(high-temperature area) to 2.23 % (low-temperature area) extreme for most vent zone inhabitants seems to be about
(Bogdanov et al., 2004) and reaching up to 6.21% in some 25-40°C. A few prominent zones can be identified in the
deposits saturated with hydrocarbons (Peresypkin, personal Guaymas Basin’s hydrothermal vent field, each of which is
communication). More than a hundred high-temperature dominated by certain megafaunal groups: 1) the euthermal
hydrothermal mounds (black smokers) in an area of 30 km2 or shimmering water zone (ambient temperature of about
were discovered and described by Lonsdale et al. (1980). 25-30°C), where vestimentiferans commonly live; 2) the
Sulfide chimneys commonly grow through overlying oligothermal zone (temperatures of 3-6 to 25°C), which
sediments and can reach heights of more than 25 m. High- is populated by vesicomyid clams and mytilid mussels;
temperature fluids (maximum temperatures of up to 315°C) 3) the periphery of the vent zone (near-field, with very
are emitted from the vents into the surrounding water. Warm low or absent temperature anomalies), where specialized
fluids flow through the chimney walls and ascend past the suspension-feeders consuming bacteria are the predominant
sedimentary cover, which is enriched with organic matter. taxa; and 4) the periphery of the vent zone (far-field, without
This leads to a complicated transformation of organic matter temperature anomalies), which is occupied by non-vent
into hydrocarbons and methane (Von Damm et al., 1985) suspension-feeders (Galkin, 2002).
that is characteristic of the Guaymas Basin fluids compared Abundant settlements of vestimentifera Riftia pachyptila,
to other known vent fields. reaching up to 1 m length and occupying areas of up to
34 Demina et al.

hundreds m2, were detected in the shimmering water at the plastic bags until analysis.
hydrothermal chimney surfaces. The basic group of fauna
inhabiting the soft sedimentary cover is the vesicomyid 2.3. Pretreatment and chemical analysis of samples
clam Archivesica gigas whose settlements can accumulate
up to hundreds specimens per m2. These communities of The animal samples (ranging from 10 to 50 mg in
organisms are nutritionally dependent on the chemosynthetic weight) were carefully powdered and digested with a 1 ml
bacterial community and are typically surrounded by mixture (2:1) of ultra pure Merck concentrated nitric acid
accumulations of the bivalve mollusks Nuculana grasslei (69% v/v) and 30% hydrogen peroxide in Teflon vessels
(Allen, 1993). Sediments soaked with hydrocarbons serve with MWS-2 microwave system (Berghof, Germany).
as a substratum for these organisms. Chimney walls and Before analytical measurement, the water samples of fluids
bases are inhabited by Munidopsis alvisca crabs (predator), and the obtained solutions of digested tissues were diluted
Spongia (filter-feeder) and Phelliactis pabista (filter-feeder to 1:5 and 1:10, respectively, using high purity deionized
and predator). The latter were often attached to the shells water. The concentrations of the chemical elements in fluids
of the vesicomyid clam Archivesica gigas. Thick bacterial were determined by atomic absorption spectrophotometry
mats (with a thickness of up to a few cm) cover significant using a KVANT-2A instrument (flame version) and a
areas (hundreds of m2). KVANT-ZETA instrument (graphite furnace version) at the
P.P. Shirshov Institute of Oceanology (Moscow, Russia) of
2.2. Fluid and animal collection the Russian Academy of Sciences. Some elements were
determined by instrumental neutron activation analysis at
The material studied involved water samples taken from the V.I. Vernadsky Institute of Geochemistry and Analytical
the habitat of the vestimentifera Riftia (two shimmering water Chemistry (Moscow, Russia) of the Russian Academy of
samples from St. 4700, at 27°00’48 N, 111°24’74 W) as well Sciences. The details of the analytical methods employed
as from the habitat of the vesicomyid clam Archivesica are given in Table 1. The detection limits for flameless AAS
gigas (two water samples from the low temperature diffuser measurements were 0.5 µg l-1 (Ag), 0.7 µg l-1 (As), 0.1
habitats St.4709 (26°00’34 N, 111°24’78 W). Twenty-five µg l-1 (Cd and Cu), 0.2 µg l-1 (Co and Cr), 0.1 µg l-1 (Fe),
samples of different organs and tissues from the dominant 0.2 µg l-1 (Mn), 1 µg l-1 (Sb and Se) and 0.05 µg l-1 (Zn).
bottom organisms were also collected in the Guaymas Basin Standard solutions for metal determination were prepared
vent field (Figure 1). These samples were taken during using certified State Standard Samples (GSO). Accuracy of
the 49th cruise of the Russian research vessel “Akademik the analysis was controlled through the use of international
Mstislav Keldysh” (16-20 October, 2003) using the “Mir- reference materials: NIST SRM 2976 (mussel tissue),
1” and “Mir-2” manned submersibles. Water samples were IAEA MA-A-2/T (fish flash) and GSD-7. A comparison
collected by the “Mir” submersibles using 700 ml titanium of the metal concentrations of certified standard reference
syringes designed for sampling of hot fluids. Aboard the materials with the measured values revealed a percentage
ship, the samples were immediately filtered trough a 1 µm recovery rate of between 92-95% for Cu, Fe, Mn and Zn;
pore size nucleopore filter and placed afterwards into acid- 86-90% for Ag, Cd, Co, Cr and Pb; 82-85% for Hg, Sb,
washed high density polyethylene bottles and acidified to and Se. Determination of organic carbon was carried out
pH 2 with nitric acid (super pure MERCK). Water samples in 14 samples using a Carbon Express-Analyzer AN-2975
were stored in the refrigerator until analysis in the stationary M; with an accuracy of 0.1 %.
laboratory, which determined the content of total dissolved
chemical elements.
The samples of bottom fauna were collected using the
“slurp-gun” and sieve nets operated by the submersibles.
Each sample was washed with deionized water aboard the Tabla 1. Analytical techniques and precision of the methods
ship to eliminate sea salts and then measured and freshly Precision
dissected into the main organs; some individuals were Elements, object Analytical technique %
taken as a whole body. The shells of mollusks and the Cu, Fe, Mg and Zn in Flame Atomic Absorption Spec-
vestimentiferan tubes were rinsed with deionized water 5
fluids trophotometry (AAS)
after being separated from the interior organs, but they Ag, As, Cd, Co, Cr, Pb, Graphite furnace AAS 12
and Sb in fluids
were not treated with a 10% solution of HNO3 (as was done
As, Au, Ba, Co, Cr, Fe, Instrumental neutron activation
by Kádár and Costa, 2006), as this could have eliminated Sb, Se in organisms analysis 15
bacterial overgrowth and extracted the adsorbed fraction Cu, Mn and Zn in Flame Atomic Absorption Spec- 8
of metals from the surfaces of these organs. This method organisms trophotometry (AAS)
of shell preparation allowed us to study the total amount Ag, Cd, and Pb in Graphite furnace AAS 10
organisms
of metals in the external organs of invertebrates, whether Cold vapor concentration - Graph-
incorporated into the shell or adsorbed onto their surface. Hg ite furnace AAS after reduction 14
The samples were dried at 60°C and stored in insulated with SnCl2
 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 35

2.4. Data treatment concentrations of up to thousands of mg kg-1), followed by

Cu (up to hundreds of mg kg-1) and Ag, As, Cr, Pb and Sb (up
Standard statistical software was used for the data to dozens of mg kg-1). Contents of Cd, Co, Hg and Se did not
treatment. The bioconcentration factor (F c) was also exceed 5 mg kg-1, while Au had the lowest content, typically
calculated accordingly to a relation: less than 0.1 mg kg-1. The differences in the maximal and
minimal contents of the pooled metals reached up to six
Fc = Cm / Cwater , orders of magnitude.
Vestimentifera Riftia is a highly specialized symbiotrophic
where Cm – metal content in the whole organism (mg and the most abundant organism the East Pacific Rise. It
kg-1 dry weight), calculated from the concentrations of inhabits shimmering waters and is nutritionally dependent
each metal in organs, constitutioning whole body of the on the reduced substances (mainly H2S) contained in the
animal, on the base of the percentage of mass of each organ, hydrothermal fluids. Chemical analysis of separate organs
and Cwater is the concentration of metal in corresponding of mature individuals (which have a tube length of up to
hydrothermal solution (mg kg-1). 51 cm) have revealed two groups of elements that can
be distinguished based on their contents: i) As, Ba, Cu,
Fe, Mn and Zn with average contents between 10 and
3. Results 450 mg kg-1 (Figure 2a); ii) Ag, Cd, Co, Cr, Hg, Pb, Sb,
and Se with average contents below 10 mg kg-1 (Figure
3.1. Heavy metals in the fauna microhabitats 2b). Different organs of Riftia show various capacities
for accumulating metals. The differences are obviously
The results of element determination for the four fluid associated with distinctions in their functions. Ag, Co, Fe
samples are listed in Table 2. Samples collected from and Hg are accumulated to a greater extent in trophosomes
shimmering water (“hot fluids” of the first type) at St. 4700 relative to the other organs. The highest Ba concentration
had a weakly acidic character (pH = 5.4), while samples was found in Riftia’s tube, which consists primarily of chitin
collected from a nearby diffuser vent (“warm fluids” of the and is covered with a thick layer of bacterial biomass. The
second type) at St.4709 were more alkaline (pH = 7.49). In highest As, Cd, Mn, Se and Zn contents were found in the
both cases, pH is rather low in comparison to ocean water obturaculae, which is the anterior lociniate (or wing) end
(usually pH 8.0-8.2; Millero, 1996). Fluids of the first type directed toward fluids. The opisthosome is the posterior
are more deficient in Mg than fluids of the second type. The end and is attached to the substratum. Relative to other
Mg concentrations of both types of fluids are somewhat Riftia’s organs it is noticeably enriched in Co, Cu and Sb.
lower than observed in ocean water. In both cases, the trace The vestimentum, which represents the middle muscular,
metal contents are much higher in the fluid samples relative collar-like part of the body, is enriched in Pb relative to other
to the reference ocean water. According to our data, fluids organs. Gonads, which are responsible for reproduction,
of the first type are enriched in As, Cr, Cu, Fe, Mn, and Pb accumulate more Cr than other organs (Figure 2b). The
relative to fluids of the second type, but deficient in Ag, Cd, highest organic carbon (Corg) content (28.53 %) was detected
Sb and Zn. The Mn and Zn concentrations show the largest in the trophosome. This occurs quite naturally due to
difference between the two types of fluids (Table 2). accumulation of endosymbiotic bacteria. Meanwhile, the
lowest Corg value (20.32 %) was found in the vestimentifera
3.2. Trace metals in the Guaymas Basin organisms tube.
The second dominant specialized taxon is the vesicomyid
Average values for metal content (mg kg-1 dry weight) clam Archivesica gigas, whose gills are the main target
in the different tissues of organisms and, in some cases, organ of Zn (3110 mg kg-1) and Cu (42.5 mg kg-1), along
the whole bodies, are presented in Table 3. The highest with very similar value of 45.54 mg kg-1 in mantle, Cr
metal contents over all the samples studied were found (21.4 mg kg-1), Co (1.3 mg kg-1), and Se (1.5 mg kg-1). The
for nutritionally important Ba, Fe, Mn and Zn (with peak content of these metals in gills is much higher (up to one

Table 2. Concentrations of elements in the water samples from the Guaymas Basin’s hydrothermal field (average ±standard deviation)

Water sample type Ag, As, Cd, Co, Cr, Cu, Fe, Mg, Mn, Pb, Sb, Zn,
nM nM nM nM nM µM µM mM µM nM nM µM
First type (n=2): hot, 2±1 700±80 2±1 190±130 760±230 0.66±0.16 20.6±2.5 34.00±1.2 43.6±3.6 41±5 30±11 0.32±0.11
pH 5.40
Second type (n=2): 26±8 100±50 4±1 160±110 470±120 0.29±0.07 7.5±1.4 43.10±2.32 1.48±0.06 16±9 50±13 18.75±1.24
warm, pH 7.49
Ocean water (Li, 1991) 0.02 22 0.7 0.03 5 0.003 0.004 52.2 0.001 0.01 1.2 0.011
36 Demina et al.

Table 3. Content (mg kg-1 dry weight) of some elements in organism tissues and whole organisms inhabited the Southern trough of the Guyamas Basin
Taxon (number of Tissue Ag As Au Ba Cd Co Cr Cu
specimens)
trophosome 3.46±1.2 7.12±1.5 0.018±0.004 34±3 1.86±0.32 3.24±1.53 1.1±0.4 15.4±2.6
obturaculae 0.62±0.23 6.3±1.8 0.019±0.005 1375±220 12.1±1.7 0.35±0.27 0.69±0.2 7.9±2.7
Riftia pachyptila (n=3), opisthosome 1.25±0.15 0.73±0.1 0.023±0.007 56±5 2.44±0.32 0.97±0.73 2.87±1.45 0.6±0.2
tube length= 10-21.5 cm
vestimentum 0.43±0.12 3.67±0.95 0.03±0.01 290±45 2.0±0.4 0.32±0.15 1.47±0.43 7.9±3.2
tube nd 3.59±1.0 0.019±0.007 335±38 4.04±0.42 1.78±0.64 5.44±1.38 11.3±3.5
trophosome 0.92 17.8 0.007 7 0.44 0.34 3.14 34.0
obturaculae 0.74 46.4 0.025 42 2.02 0.28 2.6 24.3
Riftia pachyptila (n=1), opisthosome 0.62 10.1 nd 38 0.60 2.95 0.46 42.8
tube length= 51 cm vestimentum 0.4 2.25 0.014 45 0.08 0.37 0.41 8.7
gonades 0.48 0.34 0.007 115 0.07 1.28 3.76 4.6
tube nd 1.93 nd 200 0.38 0.48 4.78 26.3
tube, posterior end 0.05 1.22 0.007 70 1.06 0.3 3.78 4.8
Riftia pachyptila (n=1), tube, middle part nd 6.25 0.037 67 0.58 0.53 0.59 21.3
tube length= 115 cm
tube, anterior end nd 28.8 0.001 185 0.44 0.36 0.78 8.6
whole soft tissues 64.0±7.3 56.3±18.2 0.034±0.013 1440±208 4.0±0.35 0.77±0.25 3.9±2.0 879±75
Nuculana grasslei (n=15)
shell 1.24±0.16 2.33±0.71 0.003±0.002 58±39 0.34±0.05 0.23±0.1 2.65±0.7 16.6±4.8
foot 0.37 3.57 0.018 73 3.62 0.41 5.57 9.2
Archivesica gigas (n=1), gills 1.22 1.01 0.024 280 1.12 1.29 21.4 42.5
shell length=73 mm
mantle 7.29 4.14 0.085 725 4.32 0.29 4.03 45.5
Archivesica gigas (n=1), shell 0.03 1.16 0.003 870 3.64 0.27 0.61 8.5
shell length=88 mm
Phelliactis pabista (n=1) whole nd 8.15 nd 140 5.70 0.28 1.29 69.7
chitin 0.81 1.92 0.003 21 2.86 0.3 0.25 51.7
Munidopsis alvisca (n=1) spawn 0.44 2.65 nd 47 0.34 0.18 0.65 39.9
remaining 1.43 3.92 0.02 125 4.32 0.36 1.72 122
Spongia (n=1) whole 0.91 9.5 0.012 225 6.64 0.97 1.67 80.7

Taxon (number of Tissue Cu Fe Hg Mn Pb Sb Se Zn Corg, %

specimens)
trophosome 15.4±2.6 785±80 1.66±0.3 10.2±3.8 0.14±0.08 4.95±1.2 0.41±0.1 255±27 24.2±2.3
obturaculae 7.9±2.7 92±8 1.21±0.42 19.3±7.5 24.6±11.3 8.19±2.0 0.93±0.23 231±27 nd
Riftia pachyptila (n=3), opisthosome 0.6±0.2 nd 4.34±1.35 10.1±2.4 1.52±0.16 0.82±0.25 1.31±0.25 410±46 nd
tube length= 10-21.5 cm
vestimentum 7.9±3.2 10±3 1.43±0.37 15.5±5.4 0.47±0.1 5.67±2.1 0.34±0.13 105±12 22.9±1.4
tube 11.3±3.5 102±14 0.41±0.23 12.2±2.5 3.65±0.93 1.44±0.2 0.26±0.1 112±13 20.3±1.7
trophosome 34.0 463 7.81 7.8 1.10 6.33 1.84 101 28.5
obturaculae 24.3 451 0.26 17.6 0.05 11.3 4.35 380 26.1
Riftia pachyptila (n=1), opisthosome 42.8 131 1.70 13.8 0.05 13.7 1.5 175 27.5
tube length= 51 cm vestimentum 8.7 110 4.36 8.6 3.00 2.09 0.37 82 27.4
gonades 4.6 62 1.54 6.1 0.47 1.72 1.55 173 25.8
tube 26.3 112 0.27 6.2 0.75 0.74 1.6 44 nd
tube, posterior end 4.8 nd 0.17 2.9 0.73 0.21 0.42 40 22.9
Riftia pachyptila (n=1), tube, middle part 21.3 215 0.31 9.5 2.45 0.52 3.79 73 21.5
tube length= 115 cm
tube, anterior end 8.6 92 0.21 5.5 3.68 4.4 1.25 42 21.1
whole soft tissues 879±75 8905±765 1.57±0.32 6.8±3.2 24.3±10.2 13.1±2.8 7.3±2.1 580±60 nd
Nuculana grasslei (n=15)
shell 16.6±4.8 101±23 0.26±0.11 5.25±2.8 1.56±0.35 0.53±0.2 0.09±0.03 4.6±1.9 0.6±0.1
foot 9.2 125 0.98 10.8 1.84 0.32 0.56 120 nd
Archivesica gigas (n=1), gills 42.5 284 0.17 8.6 1.42 1.34 1.52 3110 23.6
shell length=73 mm
mantle 45.5 452 0.44 11.5 4.1 5.4 0.54 560 nd
Archivesica gigas (n=1), shell 8.5 191 0.08 56.8 2.72 0.009 0.16 20 nd
shell length=88 mm
Phelliactis pabista (n=1) whole 69.7 8800 0.23 172.1 70.9 1.83 1.81 3317 nd
chitin 51.7 51 0.18 230.0 0.17 0.26 0.15 60 nd
Munidopsis alvisca (n=1) spawn 39.9 26 0.11 17.2 3.58 0.053 0.63 62 nd
remaining 122 107 0.25 367.5 7.06 0.36 1.07 53 nd
Spongia (n=1) whole 80.7 703 0.38 2914.9 24.7 1.11 1.81 200 16.9

n.d.- not determined (not analyzed)

 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 37


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Figure 2. Metal contents (mg kg-1 dry weight) in the different organs of vestimentifera Riftia pachyptila at the Guaymas Basin’s vent field: a) As, Ba, Cu,
Fe, Mn and Zn; b) Ag, Cd, Co, Cr, Hg, Pb, Sb and Se.
38 Demina et al.

order of magnitude higher) than in other tissues (Table 3, (Von Damm et al., 1985), which also implies that fluids
Figures 3a, 3b). are strongly diluted by seawater during their mixing. We
The metal distribution in the soft tissues of the second also cannot exclude partial precipitation of particles from
dominant bivalve mollusk Nuculana grasslei is remarkable the fluids inside a sedimentary cover during neutralization
for having very high or the highest contents of many and cooling. The Fe/Mn molar ratios are 5.0 and 0.47 for
elements, including: Fe (8904 mg kg-1), Ba (1440 mg kg-1), fluids of the first and second types respectively, with an
Cu (873 mg kg-1), Zn (580 mg kg-1), Ag (64 mg kg-1), As average Fe/Mn ratio of 2.7. This is much lower than the
(56.3 mg kg-1), Pb (24.3 mg kg-1), Sb (13.3 mg kg-1) and basalt Fe/Mn ratio (50-60), but rather close to the Fe/Mn
Se (7.3 mg kg-1). As a rule, the difference between metal of 3 for metalliferrous sediments (Dymond et al., 1973).
contents (except Mn) in the soft body compared to the shell This suggests that, due to various biogeochemical processes
was significant, reaching up to two orders of magnitude. within the sedimentary cover, the behavior of Fe and Mn
In the whole body of the Phelliactis pabista specimens, in fluids ascending through the sediment may be altered,
which were collected from areas impacted by hot shimmering resulting in enrichment of Fe relative to Mn in the first type
water, elevated contents of Cd (5.7 mg kg-1), Cu (70 mg kg- fluids or vice versa in the second type.
1
), Fe (8800 mg kg-1), Mn (172 mg kg-1), Pb (71 mg kg-1), Since hydrothermal vestimentiferas Riftia was first
and Zn (3317 mg kg-1) were found. Phelliactis pabista discovered only about 30 years ago, some features of its
were collected in the microhabitats of the vesicomyid clam metabolism are not fully elucidated. The trophosome is
Archivesica gigas. Many specimens were attached to the known to host intracellular symbiotic bacteria, performing
shells of these clams. sulfide oxidation and carbon fixation. Based on this, the
In the chitin and remaining tissues (gills) of the high Corg content (28.53 %) detected in trophosome is
Munidopsis alvisca crab, elevated concentrations of Cu (122 quite natural and can be attributed to accumulation of
mg kg-1) and Mn (367 mg kg-1) were detected. These levels endosymbiotic bacteria. A rather small difference (about 8
were higher than those observed in the organs of Munidopsis %) between the highest and lowest Corg concentrations in
alvisca prey Riftia and Archivesica gigas. the Riftia organs might be attributed, in our opinion, to the
In the whole body of Spongia specimens, collected presence of bacterial biomass in the form of microbial mats
where hot fluids were emitted, maximum Mn content and overgrowth on the Riftia tubes. The vestimentiferan
(2915 mg kg-1) was detected, approximately two orders of growth rate is known to range from 10 (Fustec et al., 1988)
magnitude higher than in the other organisms. The other to 50 cm per year (Tunnicliffe, 1991). Thus, it follows that
chemical elements studied also demonstrate rather high our examined Riftia individuals are rather young - between
concentrations in Spongia (Table 3). Sponges are filter- one (tube length 10-21 cm) and five (tube length 51 cm)
feeding organisms that utilize organic matter and bacterial years old. Our data do not allow us to examine differences
biomass as well as mineral suspensions. Their biochemical in the trace metal contents of different organs in these two
functioning and siliceous mineral skeletons lead to the groups; however, data from Ruelas-Inzunza et al. (2005)
formation of biostructures with very high porosity, which seem to show that only concentrations of Cd and Fe in
contributes to their effective adsorption and absorption vestimentum increase with the size of specimens. The
capabilities. rest of the metals did not show any relationship to length.
Ruelas-Inzunza et al. (2005) also found that the trophosome
is an organ with high accumulation of Co, Cu and Fe. Our
4. Discussion data support this conclusion for Cu and Fe. The calculation
of average metal contents in two different-sized groups of
The geochemical environmental conditions of the Riftia shows that the trophosome is a target organ for Fe
Southern trough of the Guaymas Basin apparently result in (624 mg kg-1), Cu (24.7 mg kg-1), Ag (2.19 mg kg-1) and
some peculiarities in fluid composition. In particular, Mn Hg (4.73 mg kg-1). It should be noted that our data on the
concentration is distinctly higher than Fe concentration in distribution of the majority of metals in different Riftia
hot fluids of the first type compared to warm fluids of the organs are similar in orders of magnitude to earlier published
second type. This differs from the hydrothermal vent fluids findings for the Guaymas Basin, with the exception of Cu
of the Mid-Atlantic Ridge and 9° 50’ N of the East Pacific in the opistosome, Fe in the vestimentum and Hg in the
Rise, where Fe is found in higher concentrations than Mn trophosome and vestimentum; in these cases our data are
(Douville et al., 2002; Von Damm, 2000). Magnesium is approximately one order of magnitude lower (Table 4).
completely absent in pure end-member hydrothermal fluids Using data from Tables 3 and 5 (Demina et al., 2007),
due to its uptake by basalts during hydrothermal circulation inter-site comparisons of metal content can be conducted for
(Von Damm, 1990). The relatively high Mg concentrations organisms taken from geochemically different vent fields:
in our water samples are evidence of a high degree of fluid the 9° 50’ N EPR and the Guaymas Basin. In Riftia organs
dilution with the seawater. On the other hand, the levels the Mn contents are about 3 times higher in the trophosome
of trace metals in these fluids are much lower than in the and obturaculum and 24 times higher in the tubes of the
end-member fluids of the Guaymas hydrothermal vent field Guaymas Basin’s specimens relative to specimens taken
 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 39



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Figure 3. Distribution of metals in organs of vesicomyid clam Archivesica gigas: a) Ba, Cu, Fe, Mn and Zn; b) Ag, As, Au, Cd, Co, Cr, Hg, Pb, Sb and
Se.
40 Demina et al.

Table 4. Levels of some trace elements (mg kg-1 dry weight) in the invertebrates inhabited the Guaymas Basin’s hydrothermal vent field, based on
published data

Organ Ba Cd Co Cr Cu Fe Hg Mn Pb Zn Reference

Vestimetntifera Riftia pachyptila

trophosome 98 1.9 2.8 2.9 13.8 493 n.d. 0.7 9 428 Lein et al., 1989
trophosome n.d. 1.7 2.2 3.4 26.4 521 22.2 4.1 1.9 245 Ruelas-Inzunza et al., 2005
vestimentum 74 1.5 0.1 7 27 4900 n.d. 31 <5 250 Lukashin et al., 1990
vestimentum n.d. 3.7 0.7 3.4 11.6 297 22.5 6 2 599 Ruelas-Inzunza et al., 2005
opistosome n.d. 5 n.d. 2.1 117 333 n.d. 24 n.d. 1613 Lein et al., 1989
tube 50 1 1.5 <2 16.7 420 n.d. 30.7 5.4 195 Lukashin et al., 1990

Vent clam Archivesica gigas

gills 230 11 1.5 8.3 12 400 n.d. 6.6 5 1000 Lein et al., 1989
whole soft
tissues 350 9.5 5 2.5 18 290 n.d. 11 5 200 Lukashin et al., 1990

shells n.d. 10 n.d. 6 10 54 n.d. 56 22 135 Lukashin et al., 1990

Vent clam Vesicomya gigas

gills n.d. 115.2 n.d. n.d. 8.26 403 4.96 18 2.89 845
Ruelas-Inzunza et al., 2003
mantle n.d. 12.3 n.d. n.d. 29.7 277 1.1 10.6 3.67 419

n.d. is not determined (not analyzed)

Table 5. Average content* of some elements in organs of mussels, clams and vestimentiferas from the 9°50’ degree N hydrothermal field (Demina et al.,
2007)

Taxon Organ Ag As Ba Cd Co Cr Cu Fe Hg Mn Pb Zn Сorg, %

15.44 7.50 46 4.66 42.75 5.91 166.4 214.4 0.18 4.32 0.40 120.1 27.1
gills
1.64 3.22 28 0.15 30.76 5.35 6.1 2.6 0.04 1.67 0.45 15.1 5.7
4.58 2.23 70 0.30 5.13 3.15 18.6 25.1 0.08 1.18 0.87 41.9 25.5
mantle
2.82 2.31 15 0.39 4.49 1.07 1.2 7.7 0.04 0.11 1.15 0.2 6.8
2.00 3.15 563 0.07 6.14 32.39 5.8 36.8 0.19 2.37 1.51 30.2 23.3
Bathymodiolus thermofilus foot
0.09 3.73 583 0.08 3.27 5.20 2.3 35.0 0.20 0.43 0.78 1.6 3.6
4.68 2.37 30 0.85 6.08 1.27 27.9 101.3 0.14 1.12 2.36 65.6 29.2
remaining
0.10 0.21 18 0.84 2.06 0.72 13.4 32.0 0.12 0.11 3.28 18.7 6.3
0.02 1.98 67 0.21 2.44 0.40 7.6 52.1 0.05 4.41 6.98 8.2 2.4
shell
0.00 2.16 62 0.26 0.69 0.19 4.5 2.2 0.01 2.07 3.74 5.9 1.6
gills 2.28 9.43 94 1.55 3.16 74.0 66.8 377.9 0.05 3.78 1.73 260.2 29.5
mantle 3.79 3.79 34 2.06 3.63 10.8 32.9 170.0 0.06 49.22 8.36 320 23.8
Archivesica gigas foot 4.64 4.64 30 0.12 3.42 1.54 18.3 140.0 0.07 2.53 102.1 400 28.3
remaining 7.27 3.61 23 1.1 2.45 3.19 21.4 100.8 0.04 4.17 1.61 145.1 26.0
shell 0.03 1.03 42 0.01 2.8 1.32 4.68 24.8 0.05 1.94 8.63 12 0.3
3.83 5.82 39 0.23 17.05 1.09 23.3 389.3 0.51 3.19 11.95 157.5 28.9
trophosome
4.13 1.87 15 0.19 13.48 0.70 23.8 171.0 0.22 2.45 17.71 97.9 5.1
1.52 2.13 0.72 9.42 4.62 18.9 1035 0.14 13.06 8.44 355.3 24.8
obturaculum
1.16 0.88 0.62 8.93 6.15 8.3 760.1 0.13 7.53 11.83 129.7 4.3
3.67 2.96 608 0.10 3.21 4.02 20.0 232.1 0.74 166.37 7.51 166.4 32.7
Riftia pachyptila opistosome
2.75 2.60 796 0.01 1.41 1.83 19.8 14.2 0.11 63.88 5.03 63.9 0.0
2.22 1.29 75 0.25 13.28 2.03 13.1 164.0 0.51 31.32 2.71 72.0 24.5
vestimentum
1.87 0.38 49 0.25 8.49 1.22 12.5 48.9 0.37 38.82 0.55 22.0 1.0
0.56 2.12 50 0.23 4.01 2.04 18.9 118.0 0.29 0.31 3.47 26.1 23.6
tube
0.20 0.79 14 0.27 0.49 2.15 10.1 77.5 0.19 0.02 5.45 9.4 1.6

* metal content - in mg kg-1 dry weight; for each organ the first line is average content, the second one is ± standard deviation.
 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 41

from the 9°50’ N EPR. A similar excess in Guaymas Basin’s the clam population may receive nutrients by suspension-
specimens was found for As (2 to 12 times higher), Cd (4 to feeding to a greater extent than is observed as a result of
18 times higher), and Hg (up to 9 times higher). Meanwhile symbiotrophy. In this case, in a mantle where chemical
Cu, Fe and Zn showed similar levels in both cases, but the elements are assimilated mainly from food rather than
Ag, Co and Pb contents were several times lower in the from water via gills, metals could be highly accumulated
Guaymas Basin’s Riftia specimens. A rather high standard relative to gills.
deviation of average contents of many metals obviously The shells of the vesicomyid clam Archivesica gigas
testifies the lack of significant difference in metal contents are an important target for Ba, Mn, and to a lesser extent of
in specimens of these two fields. Fe (Figure 3a), however for other metals, they play only a
A comparison of metal levels in bivalves showed that small role. Taking into account the large mass of the shell
only in the external organs (gills and shells) there is a relative to the soft tissue of clams (in which the former may
noticeable accumulation (an order of magnitude higher) of reach one order of magnitude higher that the latter), we can
essential metals (Fe, Mn and Zn) in the Guaymas Basin’s suggest that shells, which have accumulated trace metals
specimens. Hg contents in the soft tissues are 10 times higher during biomineralization and adsorption, might serve as
in Guaymas Basin’s specimens than in specimens collected a great reservoir for many metals. The second abundant
from the 9° 50’ N EPR. Contents of these metals are at bivalve mollusk Nuculana grasslei lives on substratum
similar levels in both cases for other organs. Specimens saturated with hydrocarbons (Allen, 1993). Unlike similar
from the 9° 50’ N EPR contain only three elements (As in species, this animal has an extremely thick periostratum
gills, Ag in foot and Co in mantle, foot and shell) at about 10 (an exterior part of the shell) that is considered to be an
times higher than the level of Guaymas Basin’s specimens. adaptation to functioning in an acidic environment enriched
Thus, we cannot conclude that levels of the majority in sulfides. Its nutritional source has not yet been studied
of metals in organism tissues are a reflection of their completely, but some researchers regard Nuculana grasslei
levels in the fluids, since majority of metals show much as a symbiotrophic organism containing bacteria in its gills
higher concentrations in the fluids of the 9° 50’ N EPR that can combine symbiotrophy with filter-feeding. This
hydrothermal region in comparison to the Guaymas Basin might lead to a significant bioaccumulation of a majority
(Von Damm, 2000; Von Damm et al., 1985). of metals in the whole body of Nuculana grasslei.
The gills of the vesicomyid clams are known to contain The high levels of some essential metals (Cu and Mn)
endosymbiotic bacteria. Along with symbiotrophy, a in the soft tissues of the Munidopsis alvisca crab seem to
nutritional strategy of this clam may include suspension- be caused by metabolic peculiarities as well as type of
filtering feeding. High amounts of Cd, Cu, Fe, Mn, Pb, S, feeding, namely, preying on other organisms such as the
and Zn were detected in the whole soft tissues (where gills symbiotrophic Riftia pachyptila and the clams Archivesica
have a larger contribution of biomass compared to other gigas and Nuculana grasslei. Phelliactis pabista, which are
organs) of a similar vesicomyid clam, Archivesica gigas, typically predators, can scavenge both fragments of bacterial
from 21° N at the East Pacific Rise (Roesijadi and Crecelius, mats and organic matter into the vent fields and thus might
1984). The data of Ruelas-Inzunza et al. (2003) on metal enhance their metal bioaccumulation. It is important to
distribution in different tissues of the vent clam Vesicomya note that Kádár et al. (2007) revealed trophic level-specific
gigas from the Guaymas Basin indicate that the highest variations in essential metal accumulation in the Menez
amounts of Cd, Fe, Hg, Mn and Zn were detected in the Gwen hydrothermal community of the Mid Atlantic Ridge,
gills, while highest contents of Cu and Pb occurred mainly showing a general trend of biomagnification of Cu, Fe, and
in the mantle. The difference between Cd concentrations in Zn from primary producers (endosymbiont bacteria) to
the gills and mantle did not exceed one order of magnitude, primary (symbiont reliant species and filter-feeders) and
while for the rest of the metals it was only 1.5-4 times. secondary consumers (predators and scavengers).
Slightly greater amounts of metal accumulation were shown The considerable Mn accumulation (much higher
in the gills of Archivesica gigas, relative to other soft tissues than other metals) in Spongia might be caused by the
(Lein et al., 1989; Lukashin et al., 1990). According to our predominance of Mn in the water column, influenced by
data, Ag, As, Au, Cd, Cu, Fe, Pb, and Sb are accumulated in fluids of the first type, compared to other metals. In the body
mantle to a greater extent than in the gills of the vesicomyid of Spongia, the Fe/Mn ratio is 0.24, on the same order of
clam Archivesica gigas (Figure 3). This might be reasonably magnitude as fluids of the first type (0.5).
explained by a distinguishing feature of the Guaymas As one can see from Table 3, Mn content in the majority
Basin’s environmental conditions: a significant amount of dominant organisms studied is considerably lower than
of production in the bacterial mats, covering sulfide ores Fe content (from one to two orders of magnitude). In the
(27 mg Corg m-2day-1, Lein et al., 1988) and contained in different tissues of the dominant animals vestimentifera
the upper 50 cm sedimentary layer (91 mg Corg m-2day-1, Riftia, vesicomyidae clam Archivesica gigas and bivalve
Gal’chenko et al., 1989) that is several times higher than in mollusk Nuculana, the Fe/Mn ratio varies from 0.8 to 1309.
the other hydrothermal fields. We may suppose that in such The lower values (≤20) were detected in exterior organs
an environment, which is highly enriched in organic carbon, such as the tubes of Riftia and the shells of Archivesica
42 Demina et al.

gigas. The higher values were found in the interior organs, similar to our data (Table 7).
especially those linked with endosymbiotic bacteria, which
includes the trophosome of Riftia and the gills of the clam
Archivesica gigas. The highest Fe/Mn ratio was found in the 5. Conclusions
soft tissues of the bivalve mollusk Nuculana. It should be
mentioned that Fe/Mn ratios in our fluid samples vary from The bioaccumulation of heavy metals in the Guaymas
0.47 to 5.0. This differentiation in Fe/Mn ratios seemingly Basin hydrothermal vent fields occurs under very specific
reflects the different forms (or species) of Fe and Mn, which biogeochemical conditions associated with thick sedimentary
determine their bioavailability. Due to its slower oxidation- cover, high biological productivity and high bacterial
reduction kinetics, Mn is able to exist in the dissolved form production of organic carbon. In such conditions, the target
of Mn (+2) longer than Fe, where it is utilized by bacteria organs of many metals are not only organs containing
and involved in relatively rapid microbially catalyzed Mn endosymbiotic bacteria (the trophosome of vestimentifera
oxidation followed by formation of bacterial aggregates Riftia or the gills of vesicomyid clam Archivesica) but also
that are not commonly assimilated by benthic organisms other organs of these organisms (such as the obturaculae and
(Campbell et al., 1988). Bacterial aggregates are taken up opisthosome of Riftia and the mantle of Archivesica) and
by zooplankton, followed by excretion of the Mn-enriched even other taxonomic groups of invertebrates (Phelliactis
fecal pellets found in the settling material taken by sediment pabista , Sponge, Munidopsis alvisca) that do not bear
traps (Tambiev and Demina, 1992). Possibly, this process endosymbiotic bacteria. Possibly due to a combination
may lead to additional enrichment in Mn of the surface of symbiotrophy with suspension-feeding, the body of
sediments, which in turn provides the benthic flux of Mn. the bivalve mollusk Nuculana grasslei is highly enriched
Studies of the trace metal levels of marine mollusks relative to the shell in all the metals studied. While the
from areas of the Gulf of California influenced by mining, lowest contents for a majority of metals were found in the
agriculture and urban activities have shown that areas that shells of clams, however the masses of the shells as a rule
are apparently pristine or have few anthropogenic activities are much higher than those of the soft tissues, and for the
have a higher content of metals such as Cu, Fe and Pb mentioned reason we suggest that shells might serve as a
in soft tissues (Table 6) (Cadena-Cárdenas et al., 2008). great reservoir for many metals.
Comparison of these data with levels of metal content in Based on the variability of Fe/Mn molar ratios in
the soft tissues of Nuculana grasslei presented in this paper diluted fluids and different tissues of organisms from the
allows us to conclude that Pb and Hg levels in mollusks hydrothermal vent areas, we can assume that Fe and Mn
from the Guaymas Basin are almost one order of magnitude are subjected to a fractionation during bioaccumulation
higher than the levels observed in mollusks from polluted processes. The apparent reason for this behavior might
areas of the Gulf of California, whereas Fe, Zn, and Cu be the different chemical speciation of Fe and Mn, which
did not reveal any significant differences. Mn contents in determine the low bioavailability of Mn for symbiotrophic
mollusks from both contaminated and pristine areas are organisms. There were no significant differences between
essentially higher than Mn contents in vent clams. In our the Cd, Cu, Fe, Hg, Pb, and Zn levels in the Guaymas Basin
opinion, this suggests the importance of the geochemical vent clams versus the bivalve mollusks from polluted areas
features of the Guaymas Basin, namely, the low fraction of the Gulf of California, which suggests the importance of
of bioavailable Mn in the water column, which leads to the heavy metal bioavailable fraction rather than their total
relatively low Mn content in the tissues of organisms content in the bioaccumulation.
despite the very high concentration of total dissolved Mn
in the microhabitat. The latter can be confirmed by the low
concentration factor Fc (ratio of metal content in an organism 6. Acknowledgments
to its concentration in the surrounding water) of Mn in the
whole body of symbiotrophic animals: Fc is only 5 and 66 The authors are grateful to the crew of the R/V 49-th
in Riftia pachyptila and Nuculana grasslei respectively cruise “Akademik Mstislav Keldysh”, Prof. Alla Lein
(Table 7). On the contrary, Fc of Mn in the filter-feeding for collection of the fluid samples, and Dr. Vyacheslav
and preying organisms reaches up to 2•103. For the rest of Gordeev for his help with the flame atomic absorption
metals Fc varies within three orders of magnitude - from 30 analyses of samples. The principal financial support for
(Co) to 3•104 (Cd). This apparently testifies a selectivity of this study was obtained from Russian Foundation of Basic
trace element bioaccumulation by the organisms which is Research, project 05-04-49413 “Trophical structure of
determined by metal bioavailability independently of metal deep-sea hydrothermal communities of the World Ocean
concentration in the water column, as well as by the feeding (reconstruction based on stable isotopes and chemical
type of taxon. Values of Fc for different organisms of the analyses)”. On the final stage of the data treatment and
vent community of the Menez Gwen hydrothermal field preparation of the manuscript this study was also partially
were from 7•103 to 8•104 for Fe, from 103 to 3•104 for Cu, supported by Mexican CONACyT - Ciencia Básica research
and from 5•103 to 2•105 for Zn (Kádár et al., 2007), being grant CB-2005-01-50421 “The evaluation of the role of
 Bioaccumulation of some trace elements in the biota of hydrothermal fields of the Guaymas Basin (Gulf of California) 43

Table 6. Levels of some heavy metal contents (mg kg-1 dry weight) in the soft tissues of the mollusks from anthropogenically polluted and pristine areas
of the Gulf of California.

Metal Range Bivalve species Area Reference

2231 - 2311 clams Chione subrugosa and Tellina sp. Pabellón-Atlata wetland system in Sinaloa Páez-Osuna et al., 1993
150 - 700 mussel M.strigata Estero de Urias, Sinaloa Ruelas-Inzunza and Páez-Osuna, 2000
85.6 - 397 clams C.gnidia and L.elatum Guaymas Bay, Sonora (contaminated area) Méndez et al., 2002
Fe 323 - 438 near the phosphorite mine La Paz
clam Megapitaria squalida Méndez et al., 2006
154 - 558 pristine (far from this mine)
189 - 572 clams Ch. californiensis, M.squalida,
L.elatum different localities of the Gulf of Cali-
fornia Cadena-Cárdenas et al., 2008
150 - 369 mussel M.edulis
25 - 1247 clam Chione californiensis
64 - 1218 clam Chione subrugosa the southern Gulf of California Páez-Osuna et al., 1993
64 - 1944 clam Tellina sp.
200 (mean) mussel M.strigata the southern Gulf of California Ruelas-Inzunza and Páez-Osuna, 2000
Zn
92.4 - 246 clams C.gnidia and L.elatum Guaymas Bay, Sonora (contaminated area) Méndes et al., 2002
up to 64,6 clam Megapitaria squalida La Paz Bay (pristine area) Méndes et al., 2006

49.8 - 91.8 clams Ch. californiensis, M.squalida,

L.elatum different localities of the Gulf of Cali-
fornia Cadena-Cárdenas et al., 2008
47.9 - 94.3 mussel M.edulis
4-5 mollusks pristine areas along the Gulf of California
mussel M.strigata, clams Chione cali-
forniensis Páez-Osuna et al., 1993
up to 82 some areas along the Gulf of California
Chione subrugosa and Tellina sp.
13.4 (mean) clams Colorado River delta García-Hernández et al., 2001
Cu
4.78 - 23.04 clams C.gnidia and L.elatum Guaymas Bay (contaminated area) Méndez et al., 2002
up to 8 clam Megapitaria squalida La Paz Bay (pristine area) Méndez et al., 2006

3.9 - 181 clams Ch. californiensis, M.squalida,

L.elatum different localities of the Gulf of Cali-
fornia Cadena-Cárdenas et al., 2008
6.1- 49.6 mussel M.edulis
0.51 - 4.03 clams C.gnidia and L.elatum Guaymas Bay, Sonora (contaminated area) Méndez et al., 2002
up to 7.8 clam Megapitaria squalida La Paz Bay (pristine area) Méndez et al., 2006
south-eastern Gulf of California, Urias
Pb 3,1 (mean) mussel Mytella strigata estuary Soto-Jiménez et al., 2008

<0.03 - 9.2 clams Ch. californiensis, M.squalida,

L.elatum different localities of the Gulf of Cali-
fornia Cadena-Cárdenas et al., 2008
0.27 - 5.8 mussel M.edulis
3.8 clam Chione californiensis
3.5 clam Chione subrugosa Pabellón-Altata wetland system in Sinaloa Páez-Osuna et al., 1993
8.7 clam Tellina sp.
0.21 - 1.28 clams C.gnidia and L.elatum Guaymas Bay, Sonora (contaminated area) Méndez et al., 2002
Cd
11.1 clam Megapitaria squalida La Paz Bay (pristine area) Méndez et al., 2006
0.42 - 4.66 clams Ch. californiensis, M.squalida,
L.elatum different localities of the Gulf of Cali-
fornia Cadena-Cárdenas et al., 2008
2.42 - 4.05 mussel M.edulis
69 clam Chione californiensis
80 clam Chione subrugosa Pabellón-Altata wetland system in Sinaloa Páez-Osuna et al., 1993
43 clam Tellina sp.
Mn 1.59 - 26.9 clams C.gnidia and L.elatum Guaymas Bay, Sonora (contaminated area) Méndez et al., 2002
14.1 (mean) clam Megapitaria squalida La Paz Bay (pristine area) Méndez et al., 2006
1.21 - 3.68 clams Ch. californiensis, M.squalida, different localities of the Gulf of Cali-
L.elatum Cadena-Cárdenas et al., 2008
fornia
0.53 - 3.12 mussel M.edulis
0-063
(mean) clam Chione subrugosa
Hg south-eastern Gulf of California Green-Ruiz et al., 2005
0.23 oyster Craassostrea gigas
44 Demina et al.

Table 7. Heavy metal content (Cm) in the whole organisms and their bioconcentration factors (Fc) at the Guaymas Basin Southern trough.

Species Feeding type Ag As Cd Co Cr Cr Cu Fe Mn Pb Sb Zn

Vestimentifera Cm 0.84 9.9 2.24 0.9 1.8 1.8 15.6 259 11.7 5.2 5.3 163
Chemoautotrophy
Riftia pachyptila Fc 4•103 2•102 104 82 45 45 4•102 2•102 5 6•102 103 8•103
Bivalve mollusk Cm 7.52 7.73 0.71 0.4 2.8 2.8 102 980 5.4 3.83 1.78 61.8
Chemoautotrophy ?
Nuculana grasslei Fc 3•103 4•102 2•103 30 102 102 1•103 2•103 66 103 3•102 50
Cm - 8.2 5.7 0.3 1.3 1.3 69.7 8800 172 71 1.8 3317
Actinia Actinaria Filter-feeding, predator
Fc - 103 104 30 50 50 4•103 2•104 2•103 2•104 3•102 3•103
Cm 0.91 9.5 6.64 1 1.7 1.7 81 703 2915 24.7 1.1 200
Sponge Spongia Filter-feeding
Fc 4•103 2•102 3•104 102 40 40 2•103 103 103 3•103 3•102 104

Cm = metal content in the whole organism (mg kg-1 dry weight), calculated from the concentrations of each metal in organs, constitutioning whole body,
on the base of the percentage of mass of each organ.
Fc = Cm / Cwater

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