Trace metal uptake by the Chinese mitten crab Eriocheir sinensis: the role of osmoregulation

https://doi.org/10.1016/S0141-1136(02)00090-9Get rights and content

Abstract

Changes in salinity affect the bioavailability and consequent uptake of trace metals by euryhaline invertebrates. In many cases, salinity-related effects on metal uptake can be explained by changes in chemical speciation but salinity may also influence uptake indirectly through its action on osmoregulatory mechanisms. Specifically, it can be hypothesised that trace metal uptake may be reduced at salinities approaching the isosmotic point of a species because, at this point, there is reduced activity of ionic exchange pumps. The present study tested this hypothesis using the Chinese mitten crab, Eriocheir sinensis, a hyper–hypo-osmoregulator with an isosmotic point around 33‰. Crabs were exposed to radio-labelled cadmium and zinc at 23, 33 and 43‰ for 4 days. To eradicate speciation effects, crabs were exposed to the same concentration of the radio-labelled free metal ion (estimated using MineQL computer software) at each salinity. Haemolymph samples were taken daily and radio-labelled metal concentrations were estimated from radioactivity counts and used to provide relative measures of metal uptake. Neither cadmium nor zinc uptake was lowest at the isosmotic point. The uptake of cadmium increased significantly with increase in salinity, while the uptake of zinc showed no significant change with increased salinity. Thus changes in trace metal uptake rates in E. sinensis do not appear to be controlled only by changes in free metal ion concentrations. The different effects of salinity change on the uptake of cadmium and zinc (in the absence of free metal ion change) also indicate that physiological responses to osmotic change alone do not control metal uptake rates for this species.

Introduction

The effects of salinity on the rates of uptake of trace metals from solution and their toxicity to aquatic invertebrates have been well documented (for reviews see Hall and Anderson, 1995, Wright, 1995). In general, uptake and/or toxicity of many trace metals are increased at low salinity indicating that the free (or aqueous) metal ion is the bioavailable form (Campbell, 1995). For example, the inorganic complexation of cadmium by chloride is necessarily decreased at low salinity due to decreased concentration of chloride ions, leaving a greater concentration of unbound (or free) cadmium (Rainbow et al., 1993, Turner et al., 1981). Increased availability of the free metal ion correlates well with the apparent increase in toxicity of cadmium at low salinity (Hall & Anderson, 1995). In addition to affecting the speciation and availability of trace metals, however, salinity also affects the physiology of invertebrates through the demands of ionic regulation. Some aquatic invertebrates (e.g. common estuarine invertebrates) respond mechanistically to salinity changes in such a way that their physiological responses interact with changes in free metal ion availabilities to control trace metal uptake rates (Chan et al., 1992, Rainbow, 1995, Rainbow, 1997). Depending on the osmoregulatory physiology of the animal, water and ions (including metals) are exchanged between the organism and the external medium at various rates in relation to the salinity of the external environment. Clearly, this adds another variable to our understanding of the mechanisms and controls of trace metal uptake in aquatic invertebrates. If metal speciation is controlled, however, rates of uptake of trace metals at various salinities can help determine the physiological processes used in metal uptake, and crustaceans have proved to be convenient models to this end (Rainbow, 1995, Rainbow, 1997).

An example of the possible control of trace metal uptake during osmoregulation has been demonstrated in the hyperbenthic mysid Neomysis integer (Wildgust & Jones, 1998). N. integer inhabits the upper reaches of estuaries and may be exposed to wide fluctuations in salinity over a single tidal cycle (e.g. Roast, Widdows, & Jones, 1998). N. integer is an extremely efficient hyper–hypo-osmoregulator, i.e. it actively regulates the ionic concentration of its body fluids irrespective of the osmotic concentration of the external environment (Moffat, 1996). Using the median lethal concentration (LC50) as a measure of toxicity, cadmium toxicity was found to be reduced at the salinity corresponding to the isosmotic point of N. integer. The authors concluded that reduced osmoregulatory ionic exchange led to decreased uptake of metal from solution, suggesting that metal uptake may be mediated by osmoregulatory mechanisms (Wildgust & Jones, 1998). A similar reduction in toxicity of cadmium at salinities close to the isosmotic point has been reported for the American mysid Americamysis bahia (DeLisle & Roberts, 1988). To test further this hypothesis the present study investigates whether the rate of uptake of cadmium or zinc is reduced at the isosmotic point of the Chinese mitten crab (Eriocheir sinensis), another hyper–hypo-osmoregulator (Scholles, 1933).

Section snippets

Materials and methods

During September 1998 and 1999, male E. sinensis were collected from the intake filter screens of Lots Road Power Station (Thames Estuary), London, UK (OS grid reference SU 266 772). Only male crabs were used in the experiments to eliminate intergender variation and the potential presence of yolk proteins in the haemolymph. Immediately after collection, the crabs were transferred to holding aquaria maintained at 33±1‰ and 10±1 °C.

Cadmium

In 1998, six, seven and four crabs from a starting number of eight survived exposure to cadmium at 22.7, 32.7 and 42.7‰, respectively; and in 1999, nine, ten and ten crabs (from ten) survived, respectively. The 1998 data for cadmium are shown in Table 1. There is a highly significant effect of salinity on cadmium uptake (ANOVA; f=15.9; d.f.=2, 14; P=0.0003). Regression analysis showed that cadmium uptake increased significantly with salinity (coefficient=0.170; t=5.77; P<0.001). However, in the

Discussion

For many trace metals, uptake and toxicity both increase at low salinity (e.g. Hall and Anderson, 1995, Wright, 1995). Furthermore, it has been shown that increased toxicity at low salinity can be explained by physicochemistry, particularly speciation of the metal ion (Rainbow, 1995, Wright, 1995), usually due to decreased complexation of the free metal ion with chloride at low salinity (Turner et al., 1981). In the present study, we have addressed how physiological responses of a crustacean to

References (25)

Cited by (0)

View full text