Trace metals in barnacles:the significance of trophic transfer

Barnacles have very high accumulated trace metal body concentrations that vary with local trace metal bioavailabilities and represent integrated measures of the supply of bioavailable metals. Pioneering work in Chinese waters in Hong Kong highlighted the potential value of barnacles (particularly Balanus amphitrite) as trace metal biomonitors in coastal waters, identifying differences in local trace metal bioavailabilities over space and time. Work in Hong Kong has also shown that although barnacles have very high rates of trace metal uptake from solution, they also have very high trace metal assimilation efficiencies from the diet. High assimilation efficiencies coupled with high ingestion rates ensure that trophic uptake is by far the dominant trace metal uptake route in barnacles, as verified for cadmium and zinc. Kinetic modelling has shown that low efflux rate constants and high uptake rates from the diet combine to bring about accumulated trace metal concentrations in barnacles that are amongst the     

Trace metals in barnacles: the significance of trophic transfer

Barnacles have very high accumulated trace metal body concentrations that vary with local trace metal bioavailabilities and represent integrated measures of the supply of bioavailable metals. Pioneering work in Chinese waters in Hong Kong highlighted the potential value of barnacles (particularly Balanus amphitrite) as trace metal biomonitors in coastal waters,identifying differences in local trace metal bioavailabilities over space and time. Work in Hong Kong has also shown that although barnacles have very high rates of trace metal uptake from solution, they also have very high trace metal assimilation efficiencies from the diet. High assimilation efficiencies coupled with high ingestion rates ensure that trophic uptake is by far the dominant trace metal uptake route in barnacles, as verified for cadmium and zinc. Kinetic modelling has shown that low efflux rate constants and high uptake rates from the diet combine to bring about accumulated trace metal concentrations in barnacles that are amongst the highest known in marine invertebrates.     

Acute dietary pre-exposure and trace metal bioavailability to the barnacle Balanus amphitrite

Rates of uptake from solution and assimilation efficiencies of the trace metals Ag, Cd and Zn were investigated in the barnacle Balanus amphitrite after exposure in the laboratory for 19 days to low and high doses of added Ag and Cd in a diatom (Thalassiosira weissflogii) diet, the major route of metal uptake in barnacles. The hypothesis under test was that acute metal pre-exposure would affect the assimilation efficiency (AE) of that and other metals and their rate of uptake from solution. It was found that pre-exposure of the barnacles to atypically high dietary challenges of Cd and Ag did not cause changes in the rates of uptake of Cd, Ag or Zn from solution. Similarly, there was no clear consistent effect of dietary pre-exposure to Cd or Ag on the assimilation efficiency of Cd, Ag or Zn. The efflux rates of the metals were also comparable following the acute dietary exposure. Subcellular fractionation data indicated that the majority of the three metals were partitioned in the insoluble fraction, with very little in the soluble fraction consisting of metallothionein-like proteins and other (heat-sensitive) proteins. The lack of induction of increased Cd or Ag AE after pre-exposure in barnacles contrasts with results for mussels; this inconsistency is interpreted to result from differences in physiological accumulation patterns, the barnacles relying to an extreme extent on insoluble detoxification.     

Interspecific comparisons of relative assimilation efficiencies for zinc and cadmium in an ecological series of talitrid amphipods (Crustacea)

A dual-labelling radioisotope technique has enabled the relative assimilation efficiencies of an essential (Zn) and a non-essential trace metal (Cd) to be determined in an ecological series of talitrid amphipods from low-shore to fully terrestrial habitats. All species exhibited high assimilation efficiencies for zinc and cadmium (within the range 66.7–96.4%). Interspecific differences in assimilation rates showed no trend with increasing terrestriality of the habitat. Elevated dietary zinc concentrations failed to enhance zinc assimilation efficiency. Incorporation of antibiotics into the diet to eliminate gut microflora did not affect zinc assimilation efficiencies. The implications of having high trace-metal assimilation efficiencies are discussed in terms of land invasion by talitrids.     

Assimilation efficiency of zinc and cadmium in the decapod crustacean Penaeus indicus

The assimilation of trace metals from food can be the main route of metal uptake into aquatic invertebrates. The assimilation efficiencies of zinc and cadmium from muscle tissue of a cephalopod mollusc (40% to 70% Zn, 64% to 83% Cd) and from a macrophytic alga (50% to 69% Zn, 39% to 50% Cd) were measured in juvenile penaeid prawns Penaeus indicus. Assimilated Zn and Cd were retained mostly in the hepatopancreas of the prawns, some metal being excreted (Zn k_e 0.10 and 0.11 and Cd k_e 0.004 and 0.009, from cephalopod muscle and alga, respectively). There were no significant differences between k_es (efflux rate constants) of one metal from either diet. Given the high trace metal assimilation efficiencies measured here, it is highly probable that metal assimilation from food plays an important role in Zn and Cd accumulation in the body of P. indicus, particularly in estuarine stages of the life cycle, for estuaries are particularly prone to metal pollution and are likely to offer the prawns abundant metal-rich diets such as detrital material derived from local macrophytes.     

Biomonitoring of heavy metals in the coastal waters of two industrialised bays in southern Spain using the barnacle Balanus amphitrite

Abstract

This paper evaluates the bioavailability of As, Cd, Cu, Mn, Hg, Ni and Zn in the coastal waters of the two most important bays in southern Spain (Cádiz and Algeciras). Concentrations of these metals were measured in the bodies of Balanus amphitrite barnacles in 2005 and 2006. Seawater samples were collected from the same sites as the barnacles to assess metal concentrations and to gain additional information on the environmental conditions. Analysis of variance (ANOVA) showed significant geographic differences in the local bioavailability of metals to the barnacles, as reflected in the concentrations of accumulated metals. Balanus amphitrite accumulates large amounts of metals, with high concentration factors for Zn, Cd, Cu and Mn, in relation to the concentrations in marine waters.     

Does the accumulation of trace metals in crustaceans affect their ecology—the amphipod example?

Crustaceans, like all aquatic invertebrates, take up and accumulate metals from a wide range of sources and the trace metal concentrations within their tissues and bodies show great variability. Trace metal uptake in crustaceans occurs from the water and food, either of which may be affected by the physico-chemical properties of the sediment. Accumulated metal concentrations in amphipods are contrasted with those of other crustaceans and examples are given to show how external and internal factors affect bioaccumulation. One of the major pathways for the uptake of trace metals is from solution directly through permeable surfaces including the gills. Changes in salinity and oxygen tension can modify the uptake characteristics from solution particularly in the case of interstitial water within sediments. Infaunal amphipods have direct contact with the sediment and the bioavailabilities of trace metals depend on the strength of the metal binding which is determined by a combination of properties including grain size, organic content, the presence of metals such as lead and iron as well as other ambient environmental conditions. Metal concentrations within amphipod bodies reflect the bioavailabilities of trace metals in their habitat. Body size is one of the major factors contributing to individual variability in trace metal concentrations within species. For some amphipod species, there are differences in trace metal accumulation with gender, breeding and developmental stage. In amphipods, accumulated body metal concentrations are the best biomarkers for environmental metal availabilities. Metal accumulation affects the ecology of crustaceans as a consequence of the energy costs associated with excreting and/or detoxifying the incoming metals. If the costs are significant, then this may result in reduced growth and reproduction. The effects of accumulated metals on communities have yet to be determined. Accumulated metals in crustacean prey species may be transferred along the food chain, but biomagnification in fish appears unlikely. One of the main ecological challenges is the need to link molecular biomarkers with ecologically relevant life history characteristics including growth, survival, reproduction and recruitment.     

Biomonitoring of trace metal contamination in mangrove-lined Brazilian coastal systems using the oyster Crassostrea rhizophorae: comparative study of regions affected by oil, salt pond and shrimp farming activities

The oyster Crassostrea rhizophorae has been used as a biomonitor of trace metal contamination in two Brazilian coastal systems. C. rhizophorae were collected in January 1998 from 15 stations (from 4 coastal inlets (including 1 estuary) and 1 coastal beach) near Macau, Rio Grande do Norte (RN), Brazil, a region affected by the activities of the oil industry and salt manufacture in coastal salt ponds; oysters were also collected in September 1999 from 8 stations in the Curimatau estuary (RN), an estuary becoming increasingly affected by shrimp farming activities. C. rhizophorae is a net accumulator of trace metals and can be used as a biomonitor, the accumulated soft tissue concentrations representing integrated records of bioavailable metal over the life of the oyster. At Macau, significant differences in oyster accumulated concentrations (and hence bioavailabilities to the oyster) of Fe, Zn, Cu, and Mn were found between stations; raised zinc availabilities at the coastal site are in close proximity to oil industry activities but the very high availabilities of Fe, Cu and Mn in the Rio dos Cavalos estuary originate from an unknown source. In the Curimatau estuary, bioavailabilities of Mn, Pb and Cd, but particularly of Cu and Zn, to the oysters are raised at the two most downstream sites, the only sites below the effluent of a large shrimp farming enterprise. The oysters also act as a local food source, and concentrations of Zn, Cu and Pb of some of the oysters are above typical public health recommended limits.     

Fluctuating asymmetry of <Emphasis Type="Italic">Amphibalanus</Emphasis> (<Emphasis Type="Italic">Balanus</Emphasis>) <Emphasis Type="Italic">amphitrite</Emphasis> (Cirripedia: Thoracica) in association with shore height and metal pollution

The level of fluctuating asymmetry (FA), which is defined as random deviations from perfect bilateral symmetry in the morphological traits of an organism, increases with increasing developmental instability, and it may be used as an indicator of environmental and/or genetic stresses. This study attempted to relate FA levels in the opercular plates of the barnacle Amphibalanus (Balanus) amphitrite with shore height and body trace metal concentrations. Barnacles were collected from both low and mid shores at six coastal locations with various degrees of marine pollution in Hong Kong. Four opercular traits, namely scutum length, tergum length, scutum width, tergum width were measured in the specimen while concentrations of five common trace metals (Cd, Cu, Cr, Mn and Zn) were determined in their body tissues using inductively coupled plasma-atomic emission spectrophotometry. Among the four traits, only tergum length and scutum width fulfilled the assumption of FA while their measurement errors were low. Across all sites, mid-shore A. amphitrite consistently exhibited a significantly higher FA level in scutum width than that in low-shore barnacles, but FA levels in tergum length were similar between the two shore heights. These results suggested that FA was trait-dependent, and mid-shore barnacles were possibly under high physical stress, such as desiccation and high temperature, leading to high developmental instability. Although no positive association was observed between FA and metal contamination in low-shore A. amphitrite, FA level in tergum length significantly increased with decreasing body concentration of manganese (Mn) in these barnacles. Such a negative relationship may be explained by the mechanism of bioaccumulation and physiological role of Mn in A. amphitrite with respect to the formation of barnacle shell plates. Handling editor: T. P. Crowe     

Development of a Marine Subtidal Epibiotic Community in Hong Kong: Implications for Deployment of Artificial Reefs

A 2-year study was conducted in Hong Kong to examine the effects of substratum, season and length of submersion on the development of a subtidal epibiotic community using four types of settlement panels (concrete, steel, wood and tyre). The season and length of submersion had a strong influence on the total biomass and on community structure while the type of substratum had very little impact on the total biomass or the structure of the epibiotic community. The season of submersion determined the species composition of the newly submerged surfaces. In the spring and summer, tubeworms were the most abundant. In the autumn and winter, barnacles and tunicates dominated. Community succession was not obvious in the first year of submersion as it was intermingled with strong seasonal settlement, growth and death of barnacles and tunicates. In the second year of submersion, green mussels and tunicates settled and grew to occupy most of the panel surfaces, forming an assemblage that was characteristic of climax communities in the local subtidal waters. The results suggest that the type of construction material has limited impact on the development of epibiotic communities on artificial reefs deployed in Hong Kong; the season of submersion may affect community structure in the early successional stage, but not the characteristics of the climax communities. This study indicates that the type of substratum should not be of concern when deploying artificial reefs in the subtidal waters in this region. The design of artificial reefs should focus more on other physical and economical aspects such as durability, flow dynamics, stability, cost, and effects on the ambient environment.     

Development of a marine subtidal epibiotic community in Hong Kong: implications for deployment of artificial reefs

A 2-year study was conducted in Hong Kong to examine the effects of substratum, season and length of submersion on the development of a subtidal epibiotic community using four types of settlement panels (concrete, steel, wood and tyre). The season and length of submersion had a strong influence on the total biomass and on community structure while the type of substratum had very little impact on the total biomass or the structure of the epibiotic community. The season of submersion determined the species composition of the newly submerged surfaces. In the spring and summer, tubeworms were the most abundant. In the autumn and winter, barnacles and tunicates dominated. Community succession was not obvious in the first year of submersion as it was intermingled with strong seasonal settlement, growth and death of barnacles and tunicates. In the second year of submersion, green mussels and tunicates settled and grew to occupy most of the panel surfaces, forming an assemblage that was characteristic of climax communities in the local subtidal waters. The results suggest that the type of construction material has limited impact on the development of epibiotic communities on artificial reefs deployed in Hong Kong; the season of submersion may affect community structure in the early successional stage, but not the characteristics of the climax communities. This study indicates that the type of substratum should not be of concern when deploying artificial reefs in the subtidal waters in this region. The design of artificial reefs should focus more on other physical and economical aspects such as durability, flow dynamics, stability, cost, and effects on the ambient environment.     

Heavy metal accumulation in tissue/organs of a sea cucumber, Holothuria leucospilota

Holothuria leucospilota Brandt, the large black sea cucumber, is a non-selective deposit feeder, and is commonly found in the bottom of shallow waters in Hong Kong, where the sediments are often polluted with heavy metals. This study was designed to test the possibility of heavy metal accumulation by the sea cucumber at two sites in Hong Kong. Atomic absorption spectrophotometer was used to measure Cu and Zn concentrations in various tissue/organs of the animal as well as in the sediments. The result indicated that H. leucospilota accumulated zinc in the longitudinal muscle bands (97.27–98.07 ppm in dry weight) and in the respiratory tree (83.92–89.64 ppm in dry weight). Copper concentrations in these two organs were much lower than that of zinc. After the animals were kept in the aquarium without sediment for40 days, zinc concentration of the longitudinal muscle and respiratory tree decreased by 48% and 39%respectively whereas copper concentration remained unchanged. The concentrations of zinc and copper in the sediment at the two sites differed significantly but the metal level in the animals from the two sites were similar, suggesting that this sea cucumber was not an ideal bioindicator of heavy metal pollution in the sediment. This revised version was published online in August 2006 with corrections to the Cover Date.     

Biomonitoring Survey of Trace Metal Pollution in Streams of a Catchment Draining a Zinc and Lead Mining Area of Upper Silesia,Poland Using the Amphipod Gammarus fossarum

We have used accumulated metal concentration data to investigate variability in the bioavailabilities of cadmium, copper, lead, zinc and iron to the amphipod Gammarus fossarum inhabiting the Biala Przemsza river system draining an area of lead and zinc mining. The highest bioavailabilities of most of the metals were found in a stream carrying water from mine drainage and flotation processes. Significant amounts of bioavailable cadmium entered via another stream receiving waters from ore processing. The bioavailabilities of copper varied little, indicating the lack of a local point source of entry. All metals other than copper showed seasonal variations with the highest concentrations recorded in October. Comparative data show the Biala Przemsza system to be contaminated with cadmium, lead, zinc and iron. The data presented exemplify metal concentration ranges in G. fossarum inhabiting industrial areas, and can be used as a reference for future surveys involving this species in Central Europe.     

Barnacle species as biomonitors of metal contamination in the northwest coast of Portugal: Ecological quality classification approach

This work discusses the simultaneous use of barnacles C. montagui and P. pollicipes as biomonitors of metal (Cd, Cr, Cu, Fe, Mn, and Zn) contamination in the northwest (NW) coast of Portugal during the four seasons of 2011. The metal concentrations in soft tissues of both barnacles species, metal bioaccumulation factors (BAFs), and ecological quality classifications of coastal waters are presented. The most and the least metal-contaminated locations were, respectively, location 5 (“Cabo do Mundo”) and location 10 (“Moledo”). The most and the least metal-contaminated seasons of 2011 were, respectively, autumn and winter. Temporal comparisons with previous works of 2009–2011 showed that C. montagui bioaccumulated Cd, Cr, and Fe at higher rates and P. pollicipes accumulated more Zn besides Cd and Fe. In addition, global mean BAFs showed that the best season to collect both barnacle species for metal contamination assessment/monitoring purposes in future works would be spring and that P. pollicipes would be the best barnacle species to monitor metals. In terms of ecological quality classification, all NW coast of Portugal should be classified as “Class III – Remarkably Polluted” due the high concentrations of Zn found in barnacles species during the four seasons of 2011. This work suggested that both barnacle species are suitable species to be included in the Portuguese Environmental Specimen Banks under European Marine Strategy Framework Directive 2008/56/EC.     

The transfer of cadmium, mercury, methylmercury, and zinc in an intertidal rocky shore food chain

We examined the transfer of cadmium (Cd), inorganic mercury [Hg(II)], methylmercury (MeHg), and zinc (Zn) in an intertidal rocky shore food chain, namely from marine phytoplankton to suspension-feeding rock oysters (Saccostrea cucullata) and finally to predatory whelks Thais clavigera. The uptake of metals from the dissolved phase was also concurrently quantified in the oysters and the whelks. Metal uptake by the oysters was not directly proportional, whereas metal uptake by the whelks was directly proportional to metal concentration in the water. The order of uptake was MeHg>Hg(II)>Zn>Cd, and was much higher in the oysters than in the whelks. The relative uptake of Zn and Cd was comparable between oysters and whelks, whereas MeHg and Hg(II) showed disproportionally higher uptake in oysters than in whelks as compared to Zn and Cd. The assimilation efficiencies (AEs) were in the order of MeHg>Zn>Cd=Hg(II) in oysters, whereas the AEs were highest for MeHg and comparable for Zn, Cd, and Hg(II) in the whelks. Pre-exposure of the oysters to different dissolved concentrations of Cd significantly elevated the AEs of Cd and Hg(II) but not of Zn, in association with the induction of metallothioneins in the oysters. The whelks significantly assimilated Cd and Zn from various prey (barnacles, oysters, mussels, and snails) with contrasting strageties of metal sequestration and storage. There was no significant relationship between the metal AE and the metal partitioning in the soluble fraction (including metallothionein-like proteins, heat stable protein, and organelles). The insoluble fraction of metals was also available for metal assimilation. Our calculations show that the dietary uptake of metals can be dominant in the overall bioaccumulation in the oysters and whelks, and the trophic transfer factor was >1 for all metals. Thus, the four metals have a high potential of being biomagnified in the intertidal rocky shore food chain. MeHg possessed the highest and Hg(II) and Cd the lowest potential of trophic transfer among the four metals considered.     

Grazing and growth responses of a marine oligotrichous ciliate fed with two nanoplankton: does food quality matter for micrograzers?

To investigate whether predator growth and grazing would depend on prey properties besides size, we studied the numerical and functional responses of a marine oligotrichous ciliate isolated in Hong Kong coastal waters, Strobilidium sp., on two nanoplanktonic preys of similar size. The growth and ingestion rates of Strobilidium sp. could be fit with prey concentrations by hyperbolic curves. Strobilidium sp. exhibited higher maximal growth rates and gross growth efficiencies, and lower maximal clearance rates on Nannochloropsis sp. than on Isochrysis galbana. Our results demonstrate that prey properties presumably food quality can have a considerable effect on predator growth and grazing and implications on phytoplankton community structure and biogeochemical cycling.     

Effects of surface fouling organisms on the occurrence of fungi on submerged pine blocks in Hong Kong coastal waters

During an investigation into the distribution of lignicolous marine fungi in Hong Kong coastal waters, pine blocks (Pinus massoniana Lambert) were used as one of the baiting substrates. The results from unscraped and scraped pine blocks showed that, in general, the presence of surface fouling organisms did not affect the pattern of occurrence of fungi either quantitatively or qualitatively. Apart from the presence of a few fungal species on the calcareous substrates provided by barnacles and shipworms, no other associations between fungi and fouling organisms were detected.     

A comparative study of chemical contamination in sediments of East River (Dongjiang) and selected reservoirs in Hong Kong

Abstract

The levels of TKN, orthophosphate, heavy metals and trace organics including total PCBs and PAHs in the sediments of the East River (Dongjiang) and various reservoirs in Hong Kong were chemically analyzed. It was found that the sediments of various sections of Dongjing and the Shenzhen Reservoir were contaminated by heavy metals at slight to medium levels. Generally speaking, the highest levels of Cd, Cu, Ni, Pb and Zn were recorded in the middle and lower tributaries of Dongjaing, particularly those near Tangxia and Guanlan. Slight amount of PCBs, PAHs were also detected in the lower sections of Dongjiang, indicating industrial contamination due to economic growth in the 1980–90s. Comparatively, only slight amounts of heavy metals were detected in the sediments of some Hong Kong reservoirs that store imported Dongjiang water. Moreover, trace organics including PCBs and PAHs were rarely detected in the reservoirs of Hong Kong. Nevertheless, the high acidity in the sediments of Hong Kong reservoirs is noteworthy. Results revealed that the Dongjiang waters were purified to a certain extent before being imported to and stored at the Hong Kong reservoirs. At present, health risks from the drinking water of Hong Kong are not apparent. However, the long-term trend of organic and inorganic contamination in Dongjiang should not be overlooked and remedial actions should be taken as early as possible. Collaboration between the governments of Hong Kong and Mainland China in tackling chemical pollution in drinking water is an example of cross-border cooperation and control measures should be stepped up as soon as possible.     

Sulfate inhibition of molybdenum-dependent nitrogen fixation by planktonic cyanobacteria under seawater conditions: a non-reversible effect

The trace element molybdenum is a central component of several enzymes essential to bacterial nitrogen metabolism, including nitrogen fixation. Despite reasonably high dissolved concentrations (for a trace metal) of molybdenum in seawater, evidence suggests that its biological reactivity and availability are lower in seawater than in freshwater. We have previously argued that this difference is related to an inhibition in the uptake of molybdate (the thermodynamically stable form of molybdenum in oxic natural waters) by sulfate, a stereochemically similar ion. Low molybdenum availability may slow the growth rate of nitrogen-fixing cyanobacteria, and in combination with an ecological control such as grazing by zooplankton, keep fixation rates very low in even strongly nitrogen-limited coastal marine ecosystems. Here we present results from a seawater mesocosm experiment where the molybdenum concentration was increased 10-fold under highly nitrogen-limited conditions. The observed effects on nitrogen-fixing cyanobacterial abundance and nitrogen-fixation inputs were much smaller than expected. A follow-up experiment with sulfate and molybdenum additions to freshwater microcosms showed that sulfate (at seawater concentrations) greatly reduced nitrogen fixation by cyanobacteria and that additions of molybdenum to the levels present in the seawater mesocosm experiment only slightly reversed this effect. In light of these results, we re-evaluated our previous work on the uptake of radio-labeled molybdenum by lake plankton and by cultures of heterocystic cyanobacteria. Our new interpretation indicates that sulfate at saline estuarine levels (>8–10 mM) up to seawater (28 mM) concentrations does inhibit molybdenum assimilation. However, the maximum molybdenum uptake rate (V _max) was a function of the sulfate concentration, with lower V _max values at higher sulfate levels. This indicates that this inhibition is not fully reversed at some saturating level of molybdenum, as assumed in a simple competitive inhibition model. A multi-enzyme, mixed kinetics model with two or more uptake enzyme systems activated in response to the environmental sulfate and molybdate conditions may better explain the repressive effect of sulfate on Mo-mediated processes such as nitrogen fixation.     

Seasonal variation in trace metal concentrations in three talitrid amphipods from the Gulf of Gdansk, Poland

Talitrid amphipod crustaceans are increasingly being used as biomonitors of trace metal bioavailabilities in coastal waters, and it is important to understand how other factors, in addition to metal pollution, might affect their accumulated body concentrations. Seasonal variation (April-October 2000) in body concentrations of copper, zinc, cadmium, iron, manganese, lead and nickel has been investigated in three species, Orchestia cavimana, Talitrus saltator and Talorchestia deshayesii, from the region of the Gulf of Gdansk (including the Vistula Lagoon), Poland, an area with considerable temperature variation between summer and winter. Seasonal variation in the body metal concentrations of talitrid amphipod crustaceans was confirmed in each population, but only copper showed a consistent pattern. Copper concentrations fell from early to late summer, perhaps either as a result of the replacement of the older overwintering generation by the younger spring one, or as a result of the loss of haemocyanin in autumn amphipods entering a period of low metabolic activity. Metal concentration data for T. saltator from Gdynia-Osada Rybacka compared with equivalent data for 1996 and 1998 show a significant drop in metals associated with the influx of the Vistula river water, which occurred in 1998, following a major flood event in 1997.