61 Oceanography and Marine Biology: An Annual Review, 2006, 44 , 61-83 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS SUSANNE P. BADEN* & SUSANNE P. ERIKSSON Göteborg University, Department of Marine Ecology, Kristineberg Marine Research Station, S-450 34 Fiskebäckskil, Sweden *E-mail: s.baden@kmf.gu.se Abstract This review provides an overview of the role, routes and effects of manganese in aquatic crustaceans. Manganese is a naturally abundant metal in marine and freshwater sediments where it is involved in a large number of chemical processes. Although sediments contain high natural concentrations of manganese, the potential danger to benthic organisms has been neglected in studies to date. Manganese bioavailability increases as the result of human impact and it accumulates in biota. Manganese may occur in toxic concentrations (10–20 mg l –1 ) in the bottom water of marine coastal areas after hypoxia, or more locally (e.g., close to industries) as well as in acidic lakes and aquaculture shrimp ponds. Though manganese is an essential metal, it is also an unforeseen toxic metal in the aquatic environment. Although the uptake and elimination of manganese is rapid, manganese affects processes that decrease the fitness of organisms. As manganese bioavailability increases, its uptake is predominately through the water. The midgut gland, nerve tissue, blood proteins and parts of the reproductive organs have the highest accumulation factors and are the main target tissues. The functional effects of manganese in aquatic environments are still sparsely investigated. Recent results show that the immune system, the perception of food via chemosensory organs and a normal muscle extension are affected at manganese concentrations observed in the field. Geochemical role of manganese Manganese is the 12th most common element, the fourth most abundant metal and is universally distributed in the earth’s crust and waters (Anonymous 2005). This metal is involved in a large number of chemical processes, due mainly to its redox sensitivity. The literature on manganese (Mn) geochemistry in the aquatic environment is immense (Elderfield 1976), whereas literature on the occurrence and biological effects of manganese in aquatic animals is comparatively sparse. Man- ganese concentrations in soil vary from 0.001–7 mg g –1 dry weight (dw), averaging 0.75 mg g –1 dw (Saric 1986). Ocean sediment concentrations vary from approximately 1–50 mg g –1 dw (Elderfield 1976). Since the 1800s an intensive and ongoing debate has been centred on the origin and amount of the manganese flux to the oceans. Three main sources have been identified: continental weather- ing (lithogenous origin), submarine volcanism and an upward migration in porewaters as a conse- quence of sediment diagenesis (Elderfield 1976). The anthropogenic supplies of manganese to aquatic biotopes derive mainly from mine tailings and from steel manufacturing industries where approximately 90% of total manganese is used as a deoxidising and desulphurising additive and as an alloying constituent (Saric 1986). Manganese (MnO 2 ) is also widely used in dry cell batteries (Saric 1986), as a contrasting agent for nuclear magnetic resonance tomography, and as an agri- cultural fungicide (Gerber et al. 2002). A manganese antiknock additive (methylcyclopentadienyl manganese tricarbonyl (MMT)) was introduced to Canada in 1990 to substitute for lead in fuel, 7044_C002.fm Page 61 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC SUSANNE P. BADEN & SUSANNE P. ERIKSSON 62 and since 1995 MMT has also been used in several states of the USA (Shukla & Singhal 1984, Davis 1998, Normandin et al. 2002). In the rapidly expanding shrimp farming industry of tropical regions, manganese is added to shrimp ponds in the form of potassium permanganate (KMnO4), as disinfectant, in concentrations causing potential hazards to life in the ponds and in the coastal zone close to the effluent water (Gräslund & Bengtsson 2001, Visuthismajarn et al. 2005). Manganese becomes bioavailable as Mn(II) in water when it is reduced by hypoxic/anoxic conditions in sediment. The reduction of manganese dioxides occurs during the degradation of sedimenting organic matter (Dehairs et al. 1989). The process is directly or indirectly microbially mediated but is fastest when sulphide and Fe(II) are reductants (Johnson et al. 1991). In general, the solubility (and bioavailability) of manganese increases with decreasing oxygen tension and pH, but not with increasing temperature (Wollast et al. 1979, Faust & Aly 1983). During oxic conditions in bottom water, sediment porewater may contain Mn concentrations of 0.16–24.0 mg l –1 (Canfield et al. 1993, Aller 1994, Magnusson et al. 1996), whereas bottom water concentrations are between 0.18–16.5 µ g l –1 (Laslett & Balls 1995, Hall et al. 1996). During hypoxia (O 2 < 3 mg l –1 )), the Mn(II) of the bottom water can increase by several orders of magnitude to 1.5 mg l –1 , as in the Kiel Bight (Balzer 1982), and up to 22 mg l –1 in the anoxic bottom water of the Orca Basin in the Mexican Gulf (Trefry et al. 1984). This review aims to give an overview of the role of manganese in aquatic animals, its routes of uptake, and biological effects, mainly focusing on marine crustaceans living in and on the sediment. As the biological chemistry of manganese is poorly explored in invertebrates, the relevant medical and biological literature on basic processes involving Mn in vertebrates is cited. Biological role of manganese Essentiality Manganese is an essential trace metal for metabolism belonging to the borderline elements (Mn, Fe, Co, Ni, Cu, Zn, Cd, Hg, Pb) of the periodic table. It lies between the oxygen-seeking elements of class A (Na, Mg, K and Ca being the most abundant) and the sulphur- and nitrogen-seeking elements (including heavy metals like Ag, Au and Hg) of class B, and thus exhibits aspects of both classes (Nieboer & Richardson 1980). In its divalent form, Mn(II), manganese has a relatively high affinity for sulphur or nitrogen in functional groups of proteins and other molecules, which enables Mn to interfere in a wide spectrum of biological processes (Simkiss 1979, Williams 1981). The divalent Mn(II) exchanges water and ligands rapidly and the binding constant of the metal in proteins is weak. Manganese is important as a cofactor or activator of different enzymatic reactions (e.g., electron- transfer reactions, antioxidant defences, and phosphorylation) (Simkiss & Taylor 1989). In the case of enzymes containing metal ions (mainly Mg(II), Mn(II) and Zn(II)) the metal ion itself can bind with groupings in the substrate and act as a strain-producing agent by forming a chelated interme- diary compound. At the same time the metal ion, because of its positive charge, is an efficient electrophilic agent that can act as an effective participant in the reaction (White et al. 1973). Examples of enzymatic reactions having Mn as an activator are acetyl-CoA carboxylase (the first reaction in the fatty acid formation in the endoplasmatic reticulum), pyruvate carboxylase (in the mitochondrial formation of oxaloacetate), glycylglycine dipeptidase (in the degradation of dena- tured intracellular proteins) and the well-known Mn-super oxide dismutase (Mn-SOD) (a redox enzyme in the mitochondria facilitating the production of dioxygen) (Cotzias 1958, White et al. 1973, da Silva & Williams 1991). Manganese is mainly accumulated in organelles like the mitochondria, Golgi apparatus and vesicles, whereas concentrations in the cytoplasm are relatively low. These concentration gradients are sustained by metal transporters over the membrane (e.g., Luk & Culotta 2001). The elimination 7044_C002.fm Page 62 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS 63 of Mn(II) from the mitochondria is a slow, energy-requiring, Na-dependent efflux mechanism (Gavin et al. 1999). In general, those metals having an essential biochemical role, such as the metals mentioned above, are regulated at the individual level, while for non-essential metals such as mercury (Hg), cadmium (Cd) and silver (Ag) there is only weak evidence of controls on accumulation. Under constant ambient conditions, the net balance between inward and outward fluxes of metals provides the underlying control on tissue burdens and, in general, metals that exchange rapidly tend to be accumulated less efficiently than metals that exchange slowly. Accumulation may give rise to body concentrations in excess of four orders of magnitude above background in non-regulating organisms (Rainbow 1992, 1997). Toxicity Many borderline metals are thus essential to metabolism as micronutrients but may have the potential of being toxic in high concentrations. The toxicity of manganese has been known for over 150 years after it was recognised that mine workers inhaling dust rich in Mn developed ‘manganism’ (Couper 1837). Manganism is an irreversible brain disease with prominent psychological and neurological disturbances. Such neurological responses have received close attention because they resemble several clinical disorders collectively described as ‘extra pyramidal motor system dys- function’ and in particular Parkinson’s disease. The disease is regarded as chronic and the clinical signs of intoxication include many symptoms dominated by speech disturbance, compulsive actions and motor dysfunction like tremor and stiff gait (Mena et al. 1967, Iregren 1990, Aschner & Aschner 1991). Recently, however, a manganese-induced epileptic syndrome was cured after treatment with a chelating treatment of CaNa 2 EDTA (Hernandez et al. 2003). Another much debated theory connects excess Mn exposure with the initiation of transmissible spongiform encephalopathy (TSE), also called scrapie in sheep and Creutzfeldts Jacobs disease (CJD) in humans. Imbalance of Mn and Cu is established when Mn- and Cu-chelating insecticides (organo-phosphates) are taken up at the same time, giving a substitution of Cu with Mn as Mn(III) in the CNS prion protein. This substitution conforms the prions, preventing their degradation, and TSE may develop (Purdey 2000). As Mn(III), manganese is able to accumulate in the brain, likely carried through the blood- brain barrier via transferrin and receptor-mediated endocytosis (Simkiss & Taylor 1989, Aschner & Aschner 1991). Transferrin is a protein containing a Fe-cluster crucial for absorption, transport, storage and excretion of Fe in mammals and is able to cross the otherwise relatively impermeable blood-brain barrier. Manganese may mirror Fe and bind to transferrin, not necessarily replacing Fe, and in this way passes the blood-brain barrier (Aschner & Aschner 1991). Within the brain the main part of Mn(III) appears to release from transferrin and concentrate in certain parts via axonal transport (Henriksson et al. 1999). In freshwater crayfish a structural analogue to the vertebrate blood-brain barrier called the glial perineurium, has been identified. The glial perineurium ensures protection of the CNS by having a high degree of ion selectivity and regulation (Butt et al. 1990). A direct uptake from the media through the nasal chamber in rats and olfactory chamber of pike (Esox lucius) followed by axonal transport along primary and secondary neurones into the olfactory bulb has been documented (Tjälve et al. 1995, 1996). A similar uptake and transport into nerve tissue of invertebrates has not been described to date. Hydrated Mn has an ionic ratio close to that of Ca(II), and its ability to affect various aspects of neuronal transmission has been ascribed primarily to its mimicry of Ca (Aschner & Aschner 1991). Manganese ions are known to affect various steps in the chemical synapses of nerve-muscle transmission in a wide range of animal groups. At low concentrations, Mn ions have been found to pass through Ca channels in a number of different preparations, e.g., giant squid axons (Yamagishi 1973), mammalian cardiac muscle (Ochi 1970, 1975; Delahayes 1975), mouse oocytes (Okamoto et al. 7044_C002.fm Page 63 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC SUSANNE P. BADEN & SUSANNE P. ERIKSSON 64 1977), starfish eggs (Hagiwara & Miyazaki 1977), larval beetle skeletal muscle fibres (Fukunda & Kawa 1977) and frog skeletal muscle fibres (Palade & Almers 1978). However, at higher concen- trations Mn ions are potent inhibitors of synaptic transmission (Katz & Miledi 1969, Ross & Stuart 1978, Xiao & Bevan 1994) and also act as competitive inhibitors of Ca ion flow through calcium channels in muscle membranes (Fatt & Ginsborg 1958, Hagiwara & Takahashi 1967, Takeda 1967, Mounier & Vassort 1975). Manganese affects not only the presynaptic site of action but also the postsynaptic site (Katz & Miledi 1969). This is consistent with earlier studies on the excitation- contraction coupling mechanisms in crustacean muscles, which indicated that Mn ions compete with Ca ions to pass through sarcolemmal calcium channels and thus affect muscle membrane depolarisation (Fatt & Ginsborg 1958, Hagiwara & Nakajima 1966, Chiarandini et al. 1970, Mounier & Vassort 1975). More recently, Hirata (2002) presented evidence that Mn(II) can induce DNA fragmentation, a biochemical hallmark for apoptosis, in neuronal cells. Deficiency The theoretical requirement of manganese for crustaceans has been calculated to be 3.9 µ g Mn g 1 dw (White & Rainbow 1987). The calculation was based on the animals’ total content, thus including the exoskeleton where the majority of the manganese is incorporated into the calcareous matrix. In the literature pelagic crustaceans are reported to have an average muscle and midgut gland concentration of less than 2 µ g Mn g –1 dw and a total manganese body concentration of 1.2–1.4 µ g Mn g –1 dw (Table 1). Even the benthic lobster Nephrops norvegicus from the pristine Faeroe Islands contains very low Mn concentrations (Table 1). When excluding the exoskeleton and the stomach (which may contain sediment rich in Mn) in these animals, the rest of the body (the soft tissue) contains an Mn concentration of 2.5 µ g Mn g –1 dw (n = 32) (S.P. Eriksson & S.P. Baden, unpublished observations). The theoretical required concentration of manganese in the soft tissue of crustaceans is thus likely to be somewhat overestimated. Since no data exist on crustacean manganese deficiency, the precise Mn requirements of Crustacea remain unresolved. It is hoped that further investigations will provide an answer. Most field-caught animals contain manganese concentrations well above the assumed basic requirements needed and manganese deficiency does not appear to pose a general threat to aquatic crustaceans (Table 1). Manganese in Crustacea — Overview Manganese is an essential metal and is thus required in at least a minimum concentration for an animal to be able to fulfil its metabolic functions. When discussing the basic body requirements of manganese, it is, however, also important to differentiate between metabolically active soft tissues and relatively inert tissues. Each tissue is likely to have its own kinetics (reaction rate) of metal uptake and loss, the determination of which can often be valuable when interpreting the biological significance of metal burdens. The interpretation of animal kinetic data and animal metal concen- tration is potentially complicated by a combination of factors including organism condition, growth, food supply, moulting and reproduction cycles, and may also depend directly or indirectly on environmental conditions like temperature, oxygen saturation and metal concentration. Some tissue metal concentrations are maintained within a narrow range and for others there may be less tight regulation and even storage. Clearly, under such circumstances, increased metal burdens in specific tissues could easily be obscured when analysing whole organisms. The literature on background manganese concentrations in different crustaceans derives from field-collected animals from marine and freshwater environments (Table 1). Average total Mn con- centration was 63 µ g Mn g –1 dw, with the lowest concentrations found in marine pelagic crustaceans and benthic lobsters from the pristine Faroe Islands. The highest total Mn concentration was found 7044_C002.fm Page 64 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC 65 ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS Table 1 Manganese concentrations found in field-caught crustaceans from pristine areas Habitat/Order/Species Subhabitat Total Eggs Exo. Gills Haem. Midg.gl. Muscle Ovary Testes References Marine Amphipoda Talitrus saltator S,B 25.2–97.4 Rainbow et al. 1998, Fialkowski et al. 2003 Thoracica Balanus crenatus ( – shell) S,B 53 Rainbow et al. 2002 Tetraclita squamosa ( – shell) S,B 6.7–10 Blackmore 1999, Rainbow & Blackmore 2001 Stomatopoda Squilla mantis D,B 32 Blasco et al. 2002 Decapoda Acantephyra eximia D 12.3* Kress et al. 1998 Aristeus antennatus D 27.9* 0.9–7.4 Kress et al. 1998, Drava et al. 2004 Bythograea thermydon D,H 0.4–1.6 Baden & Childress unpublished Callinectes sapidus S,B 36–76 14–17 3.6–4.3 Weinstein et al. 1992 Cancer irroratus S,B 36 10 10–28 7–42 0.2–0.3 7–18 2.5–5.0 6 Martin 1974, 1975, 1976, Martin & Ceccaldi 1976 Carcinus maenas S,B 74–206 92–286 175–282 0.36–0.38 7.5–10 10–24 3.1–19 Martin 1975, Bjerregaard & Depledge 2002 Heterocarpus vicarius D,B 0.4–0.6 Hendrickx et al. 1998 Nephrops norvegicus D,B 91.7 5.5–120 150 45 1.4 11 3.1 5.5 33 Eriksson & Baden 1998, Eriksson 2000a,b Nephrops norvegicus (Faroe islands) D,B 8.0 3.5 11 5.9 0.12 4.7 1.9 5.3 25 Eriksson unpublished, Eriksson & Baden 1998 Pandalus borealis D,B 5.1* Heu et al. 2003 7044_C002.fm Page 65 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC SUSANNE P. BADEN & SUSANNE P. ERIKSSON 66 Table 1 (continued) Manganese concentrations found in field-caught crustaceans from pristine areas Habitat/Order/Species Subhabitat Total Eggs Exo. Gills Haem. Midg.gl. Muscle Ovary Testes References Panulirus inflatus D,B 11 9.4–13 5.4–11 1.1–2.0 3.1 1.9 Paez-Osuna et al. 1995 Melicertus (as Penaeus ) kerathurus B 0.8* Balkas et al. 1982 Polycheles typhlops D 29.3* Kress et al. 1998 Portunus pelagicus S,P 0.6 0.1 0.7–1.2* Balkas et al. 1982, Al-Mohanna & Subrahmanyam 2001 Trachypenaeus curvirostris B 3.0* Heu et al. 2003 Decapoda, Mysidacea, Euphausiacea Larvae P 1.2–4.0 Ridout et al. 1989 Freshwater Decapoda Asellus aquaticus S,B 160 Akyuz et al. 2001 Astacus astacus S,B 67 3.6 Jorhem et al. 1994 Austropotamobius pallipes B6952Gherardi et al. 2002 Cambarus bartonii S,B 52 32 11 Alikhan et al. 1990 Orconectes virilis S,B 66–106 12–33 4–8 Young & Harvey 1991 Pacifastacus leniusculus S,B 361 2 Jorhem et al. 1994 Potamon fluviatile B53305 Gherardi et al. 2002 Potamonautes warreni S,B 239 340 508 374 87 107 89 Steenkamp et al. 1994, Sanders et al. 1998 Mean 63 22 96 100 0.63 102 9 23 37 Max/min ratio 199 34 36 847 12 3740 218 35 47 Notes: All values are given as µ g Mn g –1 dry weight tissue, except for haemolymph which is in wet weight. * Values calculated from wet weight by using ww/dw ratio stated in the original papers. Abbreviations: S-shallow, D-deep, B-benthic, H-hydrothermal vent, P-pelagic, Exo-Exoskeleton, Haem-Haemolymph and Midg.gl Midgut gland. 7044_C002.fm Page 66 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS 67 in a freshwater crayfish ( Potamonautes warreni ). Highest mean tissue Mn concentration was found in the animal’s midgut gland (102 µ g Mn g –1 dw) and the lowest concentration in the muscle tissue (average 9 µ g Mn g –1 dw). All haemolymph values were presented as wet weight (ww) values and were thus compared as such, giving an average Mn concentration of 0.63 µ g Mn g –1 ww. The dw/ww ratio of haemolymph equivalent to approximately 7–17% (S.P. Baden, unpublished observations). In general, all tissue concentrations showed a high interspecies variability, with the largest difference (almost 4000-fold) found in the midgut gland of a freshwater, benthic crayfish compared with that of a marine, pelagic crab (Table 1). Due to the high interspecies variability, and the fact that often only a few of the tissues are measured in each species, caution should be made when comparing the mean tissue concentrations at the bottom of Table 1. In two cases, sufficient data were obtained to statistically compare tissue concentrations in crustaceans of different habitats. The results showed that freshwater decapods had a significantly higher Mn concentration in the midgut gland than marine decapods (one-way ANOVA, df 10, F-value 7.4, p < 0.05), but that no difference could be observed for the Mn concentration in the exoskeleton of freshwater and marine decapods (one-way ANOVA, df 8, F-value 0.34, p > 0.05). The variability within individuals (between tissues) was in comparison lower. By ranking the tissue concentrations of Mn in Table 1 for species, where more than two tissues had been measured, the following general relationship between tissues was observed: exoskeleton, gill > egg > testes > ovary, midgut gland > muscle > haemolymph. Even when animals are exposed to elevated Mn concentrations, as in environments that are polluted (industrial waste), acidic (lakes and rivers) or hypoxic (mainly eutrophic marine areas), the relative relationship between the exoskeleton, gills, midgut gland, muscle and haemolymph holds, though concentrations are higher than in animals from pristine areas (Table 2). The routes and effects of manganese In the following sections an up-to-date review on the routes and effects of manganese in crustaceans is presented. In Figure 1 the uptake of manganese from water is described as well as the accumu- lation and effects in separate target tissues. Existing data on elimination kinetics are described under the respective tissue section. Uptake of manganese from water For many organisms the key determinant that influences metal accumulation from water is the speciation of the metal. Metals are usually considered more bioavailable as free ions than as complex ligands with anions. In sea water as much as 58% of the total Mn concentration is free hydrated ions whereas 37% is complexed with chloride, 4% with sulphate and 1% with carbonate (Simkiss & Taylor 1989). Hydrated ions are clearly larger than the equivalent ions in a crystal. These hydration properties of ions in aqueous solution are important in determining the permeability and selectivity of ions crossing membranes (Simkiss & Taylor 1989). Of the borderline metals, only Mn has a sufficiently low enthalpy to be able to shed its hydration and pass through membrane channels. The uptake of divalent trace metal ions occurs mainly at permeable respiratory surfaces, for example gills, and is driven by passive diffusion via ligand binding occurring through calcium channels (Rainbow 1997). Gills Crustaceans are relatively impermeable animals, having the main part of the body covered with a calcareous exoskeleton. The uptake of ions, including metals, dissolved in water thus occurs largely 7044_C002.fm Page 67 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC SUSANNE P. BADEN & SUSANNE P. ERIKSSON 68 through the gills (Rankin et al. 1982). The diffusion over the gill membrane is dependent on the concentration gradient of free metal ions. Crustaceans may accumulate essential as well as non- essential metals above the concentration of the medium as the metals may bind to e.g., blood proteins and thus maintain an inward flux (Baden & Neil 1998). The mean Mn concentration in animals from pristine areas is 100 µ g g –1 dw, but varies from 0.6–508 µ g g –1 dw (Table 1). During hypoxia in the SE Kattegat, Sweden, in 1995, the mean gill concentration of Mn in Norway lobster (Nephrops norvegicus) increased by 30 times to 1560 µ g Mn g –1 (Eriksson & Baden 1998; Table 2). The fraction of absorbed and adsorbed Mn is poorly investigated. However, in the SE Kattegat, a black layer of precipitated Mn on the gills was observed indicating that large amounts of adsorbed Mn may occur in the field (Baden et al. 1990). The effects of the precipitated layer of Mn on respiration is not yet investigated but it may hamper a normal function and internal hypoxia may Table 2 Manganese concentrations in field-caught crustaceans from pristine, polluted (industrial waste), acidic (lakes and rivers) and hypoxic (eutrophic) areas Habitat/Order/Species Tissue Pristine Polluted Acidic Hypoxic References Marine Amphipoda Talitrus saltator Total 31 105 Rainbow et al. 1998 Thoracica Tetraclita squamosa Total (–shell) 6.7 64 Blackmore 1999 Decapoda Callinectes sapidus Gills 56 83 Weinstein et al. 1992 Midgut gland 16 29 Weinstein et al. 1992 Muscle 4.0 6.6 Weinstein et al. 1992 Portunus pelagicus Gills 0.6 1.0 Al-Mohanna & Subrahmanyam 2001 Midgut gland 0.1 1.6 Al-Mohanna & Subrahmanyam 2001 Muscle 0.7 1.9 Balkas et al. 1982, Al-Mohanna & Subrahmanyam 2001 Nephrops norvegicus Exoskeleton 223 304 Eriksson & Baden 1998 Gills 58 1560 Eriksson & Baden 1998 Haemolymph 3.3 4.3 Eriksson & Baden 1998 Freshwater Decapoda Cambarus bartonii Total 52 68 513 Alikhan et al. 1990 Exoskeleton 32 102 248 Alikhan et al. 1990, Young & Harvey 1991 Midgut gland 11 59 337 Alikhan et al. 1990 Orconectes virilis Exoskeleton 86 106 Young & Harvey 1991 Gills 23 36 Young & Harvey 1991 Muscle 6.0 4.5 Young & Harvey 1991 Potamonautes warreni Total 239 662 Sanders et al. 1998 Exoskeleton 340 1203 Steenkamp et al. 1994 Gills 508 886 Steenkamp et al. 1994 Midgut gland 374 773 Steenkamp et al. 1994 Muscle 87 168 Steenkamp et al. 1994 Notes: All concentrations are given as mean µ g Mn g –1 dry weight tissue, except haemolymph which is in wet weight. 7044_C002.fm Page 68 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS 69 develop, as has been found by Spicer & Weber (1991) for crustaceans when exposed to other essential metals like Cu and Zn. Since the gills are part of the exoskeleton, changes in Mn concentration during the moult cycle follow the same pattern in these two tissues (Eriksson, 2000a). This is further discussed in the section ‘Exoskeleton’ below. Haemolymph Having passed the gill epithelium, Mn is transported in the haemolymph to target tissues either dissolved in the plasma or bound to the haemolymph proteins, predominantly (80–90%) to the respiratory protein haemocyanin (Baden & Neil 1998). Exposing N. norvegicus to realistic con- centrations of dissolved Mn (5 and 10 mg Mn l –1 for 2 weeks) the haemolymph plasma reaches the same concentration as the ambient water, whereas the Mn concentrations of the haemocyanin and whole haemolymph (plasma and haemocyanin) are about twelve and three times higher, respectively (Baden & Neil 1998). However, when N. norvegicus were exposed to Mn concentra- tions of 60 mg Mn l –1 for 2 weeks the plasma and whole haemolymph reached only 0.5 and 1.5 times the concentration of the ambient water (Selander 1997). The biological half-life for manganese accumulation in N. norvegicus during exposure to 5 and 10 mg Mn l –1 and elimination in undosed sea water is relatively fast in haemolymph (about 24 h for both processes) (Baden et al. 1999). As the competitive binding of metals by organic ligands (the Irving-Williams series) is stronger for Cu 2+ than Mn 2+ (Rainbow 1997), Mn does not replace Cu as apostethic metal in the haemocyanin, as indicated by a constant Cu concentration with increasing Mn concentration of the haemolymph (Baden & Neil 1998). Removal and displacement of Ca from haemocyanin may change the quaternary structure and thus the functional properties of the haemocyanin (Van Holde & Brenowitz 1981, Brouwer et al. 1983). The binding of Cd and Zn is stronger than Ca and has been shown to replace Ca in the haemolymph of the blue crab, Callinectes sapidus . Even though Mn binds slightly stronger than Ca, Figure 1 Routes and effects of manganese in a crustacean. Dissolved Mn II in water may enter via the gills or antennules or get precipitated on the exoskeleton. Entrance may also occur via the food in a variety of chemical form. Octagonal boxes indicate the route and target tissues of Mn and square boxes indicate the effects of Mn exposure. Observed effects ( √ ) and hypothetical but not yet investigated effects(?). Mn (ll) Gills Midgut gland Reproductive organs Haemato- poetic tissue O 2 uptake/ respiration? Immune Suppression √ Storage √ Necrosis ? Reduced muscle function √ Fertility ? No synthesis of Hc in hypoxia √ Reduced chemo- sensitivity √ Stomach Antennulae Mn (ll)Mn Haemolymph Nerve tissue Muscle 7044_C002.fm Page 69 Monday, April 17, 2006 1:37 PM © 2006 by Taylor & Francis Group, LLC SUSANNE P. BADEN & SUSANNE P. ERIKSSON 70 no change in Ca concentration of whole haemolymph was found in Nephrops norvegicus with increasing exposure to Mn of 60 mg l –1 (Selander 1997). This constancy in the whole haemolymph, however, does not rule out the possibility that Mn has displaced Ca from the haemocyanin to the plasma. An important source of Mn in the ocean is from hydrothermal vents. The crustaceans adapted to live close to these vents may hypothetically contain a higher concentration of Mn than non-vent crustaceans. Professor J.J. Childress from the University of California, Santa Barbara, kindly provided the authors with haemolymph from a vent crab , Bythograea thermydon, which was found to have Mn concentrations between 0.44 and 1.6 µ g g –1 ww. These Mn concentrations are within the range of haemolymph concentration from non-vent crustaceans as seen from Table 1. The max- imum mean Mn concentrations of 7.35 µg g 1 ww in a field-caught crustacean (Nephrops norvegicus) is reported from the SE Kattegat following a hypoxic period in 1995 (Eriksson & Baden 1998). The effects of manganese on haemocyanin synthesis and adaptation to hypoxia are described in a subsequent section discussing the midgut gland, as this is the primary organ for haemocyanin synthesis (Taylor & Antiss 1999). The synthesis of haemocytes takes place in the haematopoietic tissue localised as a thin sheet on the dorsal site of the stomach in crustaceans (Chaga et al. 1995). The haemocytes of crustaceans consist of hyaline, semigranular and granular cells playing an important role in, for example, the innate immune defence (Ratcliffe & Rowley 1979, Söderhäll 1981, Söderhäll & Cerenius 1992). Immunotoxicology of invertebrates is an unexplored field and as a result no early investigations can be cited. Recently, Hernroth et al. (2004) discovered that when exposed to 20 mg l –1 Mn for 10 days several immunological processes of N. norvegicus were affected. The number of haemocytes decreased by 60%. Despite the great loss of haemocytes, renewal through increased proliferation of the haematopoietic stem cells did not appear to occur. Additionally, maturation of the stem cells to immune-active haemocytes was inhibited in Mn-exposed lobsters (N. norvegicus). To release the prophenoloxidase system (ProPO), which is necessary for the immune defence of arthropods, the granular haemocytes must degranulate. This degranulation activity was also significantly suppressed after Mn treatment. Furthermore, the activation of ProPO by the non-self molecule, lipopolysac- caride, was blocked. Probably Mn replaces Ca and thereby inhibits protein required for mobilisation and activation of the haemocytes. Immune suppression may explain the occurrence of shell disease caused by microbial infection of the exoskeleton in blue crab, Callinectes sapidus, from North Carolina, U.S. (Weinstein et al. 1992). The infection is related to elevated Mn concentrations in the body tissues. Similar findings might explain the high frequency of the parasitic dinoflagellate Hematodinium sp. that has been found in Nephrops norvegicus from the west coast of Scotland (Field et al. 1992). In the same area high concentrations of Mn have been recorded in the tissue of this species (Baden & Neil 1998). Midgut gland In contrast to other target tissues, where manganese accumulation reaches an equilibrium deter- mined by the exposure concentration within 5 days, the midgut gland of N. norvegicus continuously accumulates manganese at a relatively slow rate and does not reach equilibrium after a 3-week period of exposure. This slow accumulation to the hepatopancreas has also been observed for zinc in Carcinus maenas by Chan & Rainbow (1993). The elimination rate of manganese from the midgut gland is, however, much faster. The biological half-lives for accumulation and elimination of manganese are about 4 and 1.5 days, respectively (Baden et al. 1999). Insoluble granules containing metals bound with phosphorus or sulphur have been observed in the epithelial cells of the midgut gland (or comparable organ) in many invertebrates (for review see Ahearn et al. 2004). The granules scavenge and detoxify surplus metals, and are later eliminated through exocytosis. 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P.K & Mandal, A 20 04 Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review Journal of Comparative Physiology B 174, 439–4 52 Aiken, D.E & Waddy, S.L 19 92 The growth process in crayfish Reviews in Aquatic Sciences 6, 335–381 76 © 20 06 by Taylor & Francis Group, LLC 7044_C0 02. fm Page 77 Monday, April 17, 20 06 1:37 PM ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS Akyuz,... of a decapod crustacean are enhanced by flicking Science 20 5, 20 4 20 6 81 © 20 06 by Taylor & Francis Group, LLC 7044_C0 02. fm Page 82 Monday, April 17, 20 06 1:37 PM SUSANNE P BADEN & SUSANNE P ERIKSSON Selander, E 1997 Effects of hypoxia and manganese on mortality, glycogen utilisation, and calcium homeostasis of Norway lobster, Nephrops norvegicus (L.) MSc Thesis, Department of Marine Ecology, Göteborg . 61 Oceanography and Marine Biology: An Annual Review, 20 06, 44 , 6 1-8 3 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis ROLE, ROUTES AND EFFECTS. Environment, Agri- cultural Sciences and Spatial Planning (FORMAS no. 22 .3 /20 0 1-1 077) to SPB and from The Natural Swedish Research Council (VR no. 62 1 -2 00 1-3 670) to SPE. References Ahearn, G.A., Mandal,. the oxygen-seeking elements of class A (Na, Mg, K and Ca being the most abundant) and the sulphur- and nitrogen-seeking elements (including heavy metals like Ag, Au and Hg) of class B, and thus