Neotrop. Helminthol., 3(2), 2009

2009 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

REVIEW/ ARTÍCULO DE REVISIÓN

OVERVIEW OF THE STATUS OF HEAVY METAL ACCUMULATION BY HELMINTHS

WITH A NOTE ON THE USE OF IN VITRO CULTURE

OF ADULT ACANTHOCEPHALANS TO STUDY THE MECHANISMS OF BIOACCUMULATION

UNA MIRADA GLOBAL DEL ESTADO DE LA ACUMULACIÓN POR

METALES PESADOS POR HELMINTOS CON UNA NOTA EN EL USO DE CULTIVO

IN VITRO DE ACANTOCÉFALOS ADULTOS PARA ESTUDIAR

LOS MECANISMOS DE BIOACUMULACIÓN

1 2 3; 4; 1 5

Isaure de Buron ; Eric James ; Pamela Riggs-Gelasco Amy H. Ringwood Elodie Rolando & Dennis Richardson.

Forma de citar: de Buron, I, James, E, Riggs-Gelasco, P, Ringwood, AH, Rolando, E. & Richardson, D. 2009. Overview of the

status of heavy metal accumulation by helminths with a note on the use of in vitro culture of adult

acanthocephalans to study the mechanisms of bioaccumulation. Neotropical Helminthology, vol 3, Nº 2, pp.

101-110.

Key words: helminthes – acanthocephalans – bioaccumulation - heavy metals - in vitro culture -

transmission electron microscopy.

Abstract

Bioaccumulation of metals by helminths is a well acknowledged phenomenon that has triggered increasing

research interest in the past two decades and found applications in environmental studies. The ecological literature

is fairly abundant but still shows gaps with some taxa not having been studied. Variations in the ability of helminths

to sequester various metals are recognized and a synthetic overview of the literature is provided herein. Adult

acanthocephalans are known to be particularly efficient as bioaccumulators of heavy metals. We optimized an in

vitro culture technique of the acanthocephalan Moniliformis moniliformis and initiated in vitro exposure to

cadmium and lead. We propose to use this technique to study the mechanisms of uptake and sequestration of heavy

metals, which are yet to be understood.

Resumen

Palabras clave: helmintos – acantocefala – bioacumulación - metales pesados - cultivo in vitro -

microscopio electrónico de transmisión.

La bioacumulación por metales por helmintos es un fenómeno bien reconocido que ha provocado un incremento

de interés en investigación en las dos décadas pasadas y ha encontrado aplicaciones en estudios ambientales. La

literatura ecológica es bastante abundante pero aun muestra lagunas con algunos taxas que no han sido estudiados.

Variaciones en la habilidad de los helmintos para secuestrar varios metales son reconocidos y una sintética mirada

global de la literatura es proporcionada aquí. Los acantocéfalos adultos son conocidos por ser particularmente

eficientes como bioacumuladores de metales pesados. Optimizamos una técnica de cultivo in vitro del

acantocéfalo Moniliformis moniliformis e iniciamos una exposición in vitro a cadmio y plomo. Proponemos el uso

de esta técnica para estudiar el mecanismo de captación y secuestro de metales, los cuales aun deben ser

entendidos.

Department of Biology, College of Charleston, SC, USA

Department of Ophthalmology, Medical University of South Carolina, Charleston SC, USA.

Department of Chemistry, College of Charleston, SC, USA.

Department of Biology, University of North Carolina, Charlotte, NC, USA.

Department of Biology, Quinnipiac University, CT, USA.

101

INTRODUCTION

The roles of parasites in ecosystems are multiple

although too often neglected by scientists (Moller,

1987; Marcogliese & Cone, 1997; Lafferty et al.,

2008). For example, the sporadic attempts at

understanding the synergistic or antagonistic

interactions between parasites and pollutants have

(e.g., Pascoe & Cram, 1977; Brown & Pascoe, 1989)

in general been ignored by the scientific community

for decades. In short, pollution has typically been

viewed as an added stress to hosts leading to an

increased vulnerability to parasitic diseases (e.g.,

Zelikoff 1993; Arkoosh et al., 1998), or as affecting

parasites' biodiversity (e.g., Dusek et al., 1998), but

the parasites' impact proper has been ignored in

evaluating the effects of environmental pollutants

on organisms. Slowly, the complexity of the

relationship between parasitism and pollution has

begun to unravel, showing the necessity to consider

parasitism in evaluating environmental stressors

(e.g., Moller, 1987; Lafferty & Kuris, 1999; Sures &

Siddall, 1999; Schludermann et al., 2003; Sures,

2006; Hudson et al., 2006) since parasites may in

turn influence the hosts' response to pollutants by

affecting their hosts physiology and tolerance of

stressed conditions (MacKenzie, 1999;

Marcogliese, 2002; Sures et al., 2002,2003a;

Turceková et al., 2002; Sures, 2006; Sures &

Radszuweit, 2007). Ignoring parasites in

assessment of pollution on organisms is now

recognized as a potential bias in studies, which may

then lead to false conclusions (Moller, 1987; Evans

et al., 2001). Recently, another aspect of the role of

parasites in evaluating environmental pollution has

emerged via the recognition of their ability to

concentrate inorganic elements (heavy metals in

particular) at much higher levels than free-living

organisms (e.g., MacKenzie et al., 1995; Sures &

Siddal, 1999; Taraschewski, 2000). Heavy metals

are known to have a negative impact on organisms

and ecosystems (e.g, de Caralt et al., 2002; Cámara

et al., 2008; Cebrian, 2008), to bioaccumulate via

the food web (e.g., Zheng et al., 2007; Widmeyer &

Bendell-Young, 2008), and to be serious threats to

human health (e.g., Di Gioacchino et al., 2008;

Ekino et al., 2007). Hence, there is a continuous

search for bioindicators of metal pollution (e.g.,

Rainbow & Philips, 1993), including helminths, as

illustrated by the steep increase in manuscripts over

the past two decades reporting studies of host-

parasite models challenged by heavy metal

exposure [see reviews by Sures et al. (1999) and

Sures (2001, 2003, 2004].

Pioneering studies on the presence of heavy metals

in parasites occurred as early as the late 19 century

(in von Brand, 1952) as well as in the mid-late 20

century [Ince (1975, 1976) and Greichus &

Greichus (1980) worked on an ascarid, Pascoe &

Mattey (1977) studied heavy metal effects on a

metacestode, Riggs et al. (1987) examined an adult

cestode, and Brown & Pascoe (1989) cystacanths].

However, Sures et al. (1994a-c), Sures &

Taraschewski (1995) and Zimmerman et al. (1999)

may be considered the key-studies that provided the

trigger that opened up the modern field of research

into this area, which continues to attract the attention

of scientists as more and more host-parasite species

are being studied. The first models studied by these

latter workers were aquatic and involved freshwater

fish infected by adult acanthocephalans (Paratenuis

ambiguus, Acanthocephalus lucii, and

Pomphorhynchus laevis), larval A. lucii, and adult

nematodes, Anguillicolla (Anguillicoloides)

crassus. Adult acanthocephalans were shown to

accumulate high levels of lead (Pb) and cadmium

(Cd) compared to their hosts' tissues. The breadth of

studies has now expanded to brackish and marine

fish/parasite systems (e.g., Sures et al., 1997a;

Bergey et al., 2002; Sures & Reimann, 2003; Malek

et al., 2007), as well as to bird (Barus et al., 2000;

Tenora et al., 2001, 2002), mammal (Scheef et al.

2000; Sures et al., 1998, 2002, 2003b, Barus et al.,

2003) and crustacean systems (Bergey et al., 2002).

The capability to bioaccumulate various metals has

been tested further in acanthocephalans (Galli et al.,

1998; Sures & Siddall, 1999; Scheef et al., 2000;

Sures et al., 2003c; Sures & Reimann, 2003,

Zimmerman et al., 2005), nematodes (e.g., Szefer et

al., 1998; Barus et al., 2003; Sures et al., 1994, 1998;

Tenora et al., 2000; Barus et al., 2007; Genc et al.

2008), cestodes (e.g., Sures et al., 1997a,c; Barus et

al. 2000, 2003; Tenora et al., 2000, 2001, 2002;

Sures et al., 2003b; Tekin-Ozan & Kir, 2005; Malek

et al., 2007; Jirza et al., 2008) and digeneans (Sures

et al., 1998; Ryman et al., 2008). Host's tissues and

organs typically tested are muscle, liver, intestine

and may also include the gills and gonads of fish and

the kidneys in mammals. The level of concentration

Helminths as bioaccumulators of heavy metals de Buron et al.

HELMINTHS AS BIOACCUMULATORS

OF HEAVY METALS

102

of heavy metal varies depending on taxa, with

cestodes and acanthocephalans being much more

efficient accumulators than digeneans and

nematodes. Monogeneans have not been tested. It

appears also that helminths of terrestrial mammals

are not as effective at heavy metal accumulation as

those from fishes and birds (e.g., Barus et al., 2003).

However, it is necessary to modulate such a general

statement, since relatively few studies on even fewer

species have been carried out in these hosts and

because numerous factors have been detected that

affect the ability of the parasites to accumulate

metals. Such factors include the nature of the metal

itself (e.g., Sures et al., 1998), the host's age and

motility (in Tenora et al., 2000), the parasite's age

(e.g., Barus et al., 2001), stage of development (e.g.,

Brown & Pascoe, 1977; Sures & Taraschewski,

1995; Siddall & Sures, 1998), sex (in Tenora et al.,

2000), as well as, organs of the parasites examined

(Barus et al., 2000; Sures et al., 2000; Taraschewski,

2000) and the location of the parasites in the host

(Sures 1996; Sures & Siddall, 2001, 2003).

Significant interspecific (Sures et al., 1997a, 1999,

2 0 0 3 b ; B a r u s e t a l . , 2 0 0 3 ) a n d

intraspecimens/intraspecific (Szefer et al., 1998)

variations also have been found to occur.

In a nutshell in vivo adult acanthocephalans (but not

cystacanths), adult digeneans, (but not

metacercariae), and both adult cestodes and their

plerocercoids, are known to accumulate some heavy

metals. Nematodes displayed the most variation in

their ability to bioaccumulate heavy metals, with

adult philometrids (Tenora et al., 2000; Barus et al.,

2007) and adults and larvae of Anisakis (Pascual &

Abollo, 2003) being the only ones reported to be

efficient accumulators whereas other species

displayed no concentration or only little

concentration of certain metals and not others (e.g.,

Szefer et al., 1998; Tenora et al. 1999; Barus et al.,

2003; Palikova & Barus, 2003; Genc et al., 2008).

Adult acanthocephalans have been found to

accumulate Pb, Cd, chromium (Cr), silver (Ag),

nickel (Ni), and copper (Cu) (Sures et al., 1994a;

Sures & Taraschewski, 1995; Galli et al., 1998;

Sures & Reimann, 2003). In particular, Cd levels

were reported to be as high as 400 fold over control

levels and Pb levels to be as high as 2,700 fold higher

than hosts' tissues (Sures et al., 1994c).

Up to a 27,000 fold higher than water exposure

concentration has been reported (in Taraschewski,

2000). These extremely high concentrations of Cd

and Pb make acanthocephalans better bioindicators

than even the zebra mussel, Dreissena polymorpha,

which is commonly used in monitoring water

contamination (Sures et al., 1997b, 1999b).

While acanthocephalans appear to be tolerant of

these high concentrations of heavy metals, the

uptake process and accumulation in the worms is

still unexplained. It is possible that

acanthocephalans might have devised an entirely

novel mechanism to acquire heavy metals from their

surroundings. However, the available observations

suggest that uptake may be occurring via

mechanisms similar to those described for divalent

cation transport in other organisms and that this

uptake may result from a lack of discrimination

between Ca ions and heavy metal ions by the

parasite (Taraschewski, 2000).

Experiments involving activated cystacanths

exposed in vitro to Pb also showed the potential role

of bile salts in enhancing heavy metal uptake (Sures

& Siddall, 1999). However the hypothesis that the

worms absorb bile-bound heavy metals was

challenged by the fact that cadmium-exposed rats

infected by acanthocephalans had no decrease in the

amount of Cd in their tissues (Scheef et al., 2000).

These latter authors thus proposed that different

metals may have different uptake mechanisms. The

acanthocephalans' tolerance to heavy metals

indicates that they may detoxify heavy metals, as

has been suggested for other organisms (Rainbow &

Philips, 1993; Vivjer et al., 2004). Where in the

worms the metals are sequestered is not known, but

it has been suggested, as also for organisms from

other phyla, that metals are stored in the form of

intracellular granules (Rainbow & Philips, 1993).

Although not reported in acanthocephalans, this

supports the idea of Tarachewski (2000) that metals

may be stored as 'amorphous material' in the worms'

tissues.

Because the purpose of previous studies of heavy

metal intake by adult acanthocephalans was to

determine the relative accumulation of heavy metals

by the parasite and the host and to identify potential

bioindicators, these studies were performed in vivo.

ACANTHOCEPHALANS AS

BIOACCUMULATORS

IN VITRO CULTURE OF

MONILOFORMIS MONILIFORMIS

Neotrop. Helminthol., 3(2), 2009

103

Since our interest lies in understanding the

mechanisms of accumulation in these parasites we

first needed to optimize experimental conditions for

rearing acanthocephalans. Therefore, we chose to

culture adult acanthocephalans, Moniliformis

moniliformis, in vitro. Our choice was motivated by

the fact that both Cd (Scheef et al., 2000) and Pb (in

Taraschewski 2000) were reported to concentrate in

these worms compared to rat host's tissues, because

the life cycle of this species is fairly easy to maintain

in the laboratory, and because the large size of these

worms yields large amount of tissues and allowed

dissection of various organs.

In vitro culture of adult acanthocephalans had been

performed in the past but has been problematic (see

Smyth, 1990). Techniques were either cumbersome

(Nicholas & Grigg, 1965) or successful for only a

short period of time that would not be long enough

for heavy metal exposure (in Crompton & Lassière,

1984; Smyth, 1990; Polzer & Taraschewski, 1994).

Optimization of the technique of rat-collected adult

Moniliformis moniliformis and culture of individual

worms was successful for up to 8 days in Krebs

Ringer medium enriched with glucose (Sigma) at

37°C, at pH 7.2 and under 5%CO /95%N gas

2 2

conditions. Culture solution was changed once after

4 days of culture. Trial experiments involved taking

six week old worms harvested from rat duodenum

that were exposed for 4 or 8 days to lead (Pb(NO ) )

2 2

and cadmium (CdCl ) (100 µg/L, equivalent to 0.3

µM and 0.4 µM, respectively). The concentrations

of each heavy metal (mg/g dry weight) after 4 days

exposure in culture were quantified using atomic

absorption spectrometry (Fig. 1). Preliminary

results showed accumulation of both heavy metals,

with accumulated Cd levels approximately 100 fold

those of Pb. Both metals accumulated to a sufficient

degree to detect their presence in whole worms

using x-ray absorption spectroscopy (Fig. 2). Given

the insensitivity of this technique in general (a

solution spectrum requires a minimum

concentration of ~300µM metal to observe a signal),

the ability to measure this spectrum indicates a

substantial accumulation of the heavy metal within

the tissue of the worm. Structural studies are

underway to determine the in vivo coordination and

speciation of the heavy metal sequestered in the

worms. Comparison of the absorptive surface of

control worms taken from rats' intestines, control

cultured worms, and heavy metal exposed cultured

worms was done using transmission electron

microscopy (TEM) and showed that no structural

damage occurred in the worms exposed to heavy

metals (Fig. 3). We thus, propose the use of this

combination of in vitro –TEM techniques to not only

quantify heavy metals in individuals but to allow

visualization of the form they are being sequestered

in as well as their exact location in the various organs

of the worms.

Identification of the process by which these

parasites accumulate heavy metals could find

application in new techniques for detection of heavy

metals, in bioremediation, and in improved

alternative techniques to current methods of heavy

metal therapy and detoxification. The ability of

helminths to concentrate heavy metals has raised the

controversial question of whether it might be

beneficial to the vertebrate host to be infected by

these worms that appear to act as a heavy metal

sanitizer for the host (Sures & Siddall, 1999;

Taraschewski, 2000; Malek et al., 2007). However

fascinating and challenging this hypothesis is, it

must be balanced, however, by the idea that

bioaccumulation by helminths may be the reflection

of a higher ability of the host to clear heavy metals

(Szefer et al., 1998). Thus, more studies must be

carried out focusing not only on uptake pathways

but also upon sequestration mechanisms.

The authors are grateful to Carol Moskos from the

Pathology Department at the Medical University of

South Carolina for her technical help with the

transmission electron microscopy study.

Funding source: Part of this material is based upon

work jointly supported by the National Science

Foundation/EPSCoR under grant No. EPS-0132573

and National Institutes of Health/BRIN under grant

No. 8-PORR16461A. Both the National

Synchrotron Light Source and the Stanford

Synchrotron Radiation Laboratory are national

Department of Energy facilities; PRG is supported

by a grant from the Camille and Henry Dreyfus

Foundation and by the National Institutes of Health

Grant Number P20 RR-016461 from the National

Center for Research Resources

CONCLUSIONS

ACKNOWLEDGMENTS

Helminths as bioaccumulators of heavy metals de Buron et al.

104

Figure 2. XANES (X-ray Absorption Near-Edge

Spectrum) spectrum at the Pb L edge of a whole worm

III

recovered from host and cultured in media containing

-1

1000µg L of Pb salt. The spectrum was collected on a

whole worm that had been rinsed extensively to remove

any excess culture media. Data was collected at both

the Stanford Synchrotron Radiation Laboratory (SSRL)

and the National Synchrotron Light Source (NSLS) at

cryogenic temperatures (less than 30K). A solid state

Ge-detector was used to monitor the x-ray fluorescence

and scans were energy calibrated using a lead foil.

Figure 1. Concentrations of heavy metals by 8 days old adult acanthocephalans Moniliformis moniliformis

cultured in vitro four days and quantified using atomic absorption spectrometry. a: lead exposure. b: cadmium

exposure.

Figure 3. Transmission electron micrographs of the

absorptive surface of 8 days old adult acanthocephalan

Moniliformis moniliformis. a: Control worm removed

from the intestine of the rat (x 15000). b: In vitro

cultured worm for four days (x 5000). c: In vitro

cultured worm for four days exposed to100 µg/L of lead

(x 3000). d: In vitro cultured worm for four days

exposed to100 µg/L of cadmium (x 3000).

Neotrop. Helminthol., 3(2), 2009

Pb Tissue Conc (ug/g)

Cd Tissue Conc (ug/g)

105

Aarkoosh, MR, Casillas, E, Clemons, E, Kagley,

AN, Olson, R, Reno, P & Stein, JE. 1998.

Barus, V, Tenora, F & Kracmar, S. 2000.

Barus, V, Tenora, F & Sumbera, R. 2003.

Barus, V, Jarkovský, J & Prokes, M. 2007.

Barus, V, Tenora, F, Kracmar, S & Prokes M. 2001.

Bergey L, Weis JS & Weis, P. 2002.

Brand, T von. 1952.

Brown, AF & Pascoe, D. 1977.

Cámara Pellissó, S, Muñoz, MJ, Carballo, M &

Sánchez-Vizcaino, JM. 2008.

Cebrian, E. 2008.

Effect of pollution on fish diseases: potential

impacts on salmonid populations. Journal of

Aquatic Animal Health, vol. 10, pp. 182-190.

Heavy

metal (Pb, Cd) concentrations in adult

tapeworms (Cestoda) parasitizing birds

(Aves). Helminthologia, vol. 37, pp.131-136.

Relative

concentrations of four heavy metals in the

parasites Protospirura muricola (Nematoda)

and Inermicapsifer arvicanthidis(Cestoda) in

their definitive host silvery mole-rat

(Heliophobius argenteocinereus: Rodentia).

Helminthologia, vol. 40, pp. 227-232.

P h i l o m e t r a o v a t a ( N e m a t o d a :

Philometroidea): a potential sentinel species

of heavy metal accumulation. Parasitology

Research, vol. 100, pp. 929-933.

Accumulation of heavy metals in the Ligula

intestinalis plerocercoids (Pseudophyllidea)

of different age. Helminthologia, vol. 38, pp.

29-33. Mercury uptake

by the estuarine species Palaemonetes pugio

and Fundulus heteroclitus compared with

their parasites, Probopyrus pandalicola and

Eustrongylides sp. Marine Pollution Bulletin,

vol. 44, pp. 1046-1050.

Chemical physiology of

endoparasitic animals. Academic Press, New

York. Parasitism and host

sensitivity to cadmium: an acanthocephalan

infection of the freshwater amphipod

Gammarus pulex. Journal of Applied

Ecology, vol. 26, pp. 473-487.

Determination

of the immunotoxic potential of heavy metals

on the functional activity of bottlenose

dolphin leukocytes in vitro. Veterinary

Immunology and Immunopathology, vol.

121, pp. 189-198.

Ecotoxicology of heavy metals in

marine sponges: different and contrasting

effects of heavy metals on different biological

levels. In AP Svensson, (ed.). Aquatic

Toxicology Research Focus. Nova Science

Publishers, Inc. New York.

Acanthocephala. In AER Taylor & JR Baker

(eds.). In vitro methods for parasite

cultivation. Academic Press New York.

Contrasting biological

traits of Clavelina lepadiformis (Ascidiacea)

populations from inside and outside

harbours in the western Mediterranean.

Marine Ecology Progress Series, vol. 244,

pp. 125-137.

Autophagy of

hematopoietic stem/progenitor cells exposed

to heavy metals: Biological implications ad

toxicological relevance. Autophagy, vol., 4,

pp. 537-539.

Biodiversity of parasites in a freshwater

environment with respect to pollution:

metazoan parasites of chub (Leuciscus

cephalus L.) as a model for statistical

evaluation. International Journal for

Parasitology, vol. 28; pp. 1555-1571.

Minamata disease

revisited: An update on the acute and chronic

manifestations of methyl mercury poisoning.

Journal of the Neurological Sciences, vol.

262, pp. 131-144. The

effect of digeneans (Platyhelminthes)

infections on heavy metal concentrations in

Littorina littorea. Journal of the Marine

Biological Association of the UK, vol.81, pp.

349-350.

Heavy metals concentrations in

acanthocephalans parasites compared to

their fish host. Chemosphere, vol. 37, pp.

2983-2988.

Element concentrations

in the swimbaldder parasite Anguillicola

crassus (Nematoda) and its host the

European eel, Anguilla anguilla from Asi

River (Hatay-Turkey). Environmental

Monitoring and Assessment, vol. 141, pp. 59-

65.

Crompton, DWT & Lassière, OL. 1984.

De Caralt, S, López-Legentil, S, Tarjuelo, I, Uriz,

MJ & Turon, X. 2002.

Di Gioacchino, M, Petrarca, C, Perrone, A, Martino,

S, Esposito, D, Lotti, LV & Mariani-

Costantini, R. 2008.

Dusek, L, Gelnar, M & Sebelova, S. 1998.

Ekino, S. Susa, M, Ninomya, T, Imamura, K &

Kitamura, T. 2007.

Evans, DW, Irwin, SWB & Fitzpatrick S. 2001.

Galli, P, Crosa, G, Occhipinti Ambrogi, A. 1998.

Genc, E, Sangun, MK, Dural, M, Can MF,

Altunhan, C. 2008.

REFERENCES

Helminths as bioaccumulators of heavy metals de Buron et al.

106

Hudson, PJ, Dobson, AP & Lafferty, KD. 2006.

Greichus, A & GreichusYA. 1980.

Jirsa F, Leodolter-Dvorak, M, Krachler, R & Frank

C. 2008.

Ince, AJ. 1975.

Ince, AJ. 1976.

Lafferty, KD & Kuris, AM. 1999.

Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, de

Leo, G, Dobson, AP, Dunne, JA, Johnson,

PTJ, Kuris, AM, Marcogliese, DJ, Martinez,

ND, Memmott, J, Marquet, PA, McLaughlin,

JP, Mordecai, EA, Pascual, M, Poulin, R &

Thieltges, DW. 2008.

MacKenzie, K. 1999.

MacKenzie, K, Williams, HH, Williams, B,

McVicar, AH & Siddall, R 1995.

Marcogliese, DJ. 2002.

Marcogliese DJ & Cone DK. 1997.

Is a

healthy ecosystem one that is rich in

parasites? Trends in Ecology and Evolution,

vol. 21, pp. 381-385. Identification

and quantification of some elements in the

hog roundworm, Ascaris lumbricoides sum,

and certain tissues of its host. International

Journal for Parasitology, vol. 10, pp. 89-91.

Heavy metal in the nase,

Chondrostoma nasus (L. 1758), and its

intestinal parasite Caryophyllaeus laticeps

(Pallas 1781) from Austrian rivers:

Bioindicative aspects. Archives of

Environmental Contamination and

Toxicology, vol. 55, pp. 619-626.

The use of real time procedure in the

semiautomatic analysis of Ascaris

lumbricoides var. suis. International Journal

of Applied Radiation and Isotopes, vol. 26,

pp. 220-222. Some elements and their

relationships in Ascaris sum. International

Journal for Parasitology, vol. 6, pp. 127-128.

How

environmental stress affects the impacts of

parasites. Limnology and Oceanography vol.

44, pp. 925-931.

Parasites in food webs:

the ultimate missing links. Ecology Letters,

vol. 11, pp. 533-546.Parasites as pollution

indicators in marine ecosystems: a proposed

early warning system. Marine Pollution

Bulletin, vol. 38, pp. 955-959.

Parasites as

indicators of water quality and the potential

use of helminth transmission in

marinepollution studies. Advances in

Parasitology vol. 35, pp. 85-144.

Food web and the

transmission of parsites to marine fish.

Parasitology, vol. 124, pp. S83-S99.

Food webs: a

plea for parasites. Trends in Ecology and

Evolution, vol. 12, pp. 389-399.

Malek, M, Haseli, M, Mobedi, I, Ganjali, MR &

MacKenzie, K. 2007.

Moller H. 1987.

Nicholas, WL & Grigg, H. 1965.

Paliková, M & Barus, V. 2003.

Pascoe, D & Cram, P. 1977.

Pascoe, D & Mattey, DL. 1977.

Pascual, S & Abollo, E. 2003.

Polzer M & Taraschewski, H. 1994.

Rainbow, PS & Philips, DJH. 1993.

Riggs, MR, Lemly AD & Esch, G. 1987.

Ryman, JE, Van Walleghem, JLA & Blanchfield PJ.

2008.

Scheef, G, Sures, B & Taraschewski, H. 2000.

Schludermann, C, Konecny, R, Laimgruber, S,

Lewis, JW, Schiemer, F, Chovanec, A. &

Parasites as heavy

metal bioindicators in the shark

Carcharhinus dussumieri from the Persian

Gulf. Parasitology, vol. 134, pp. 1053-1056.

Pollution and parasitism in the

aquatic environment. International Journal

for Parasitology, vol. 17, pp. 353-361.

The in vitro culture

of Moniliformis dubius (Acanthocephala).

Experimental Parasitology, vol. 16, pp. 332-

340. Mercury content in

Anguilla crassus (Nematoda) and its host

Anguilla Anguilla. Acta Veterinaria Brno,

vol. 72, pp. 289-294. The effect of parasitism

on the toxicity of cadmium to the tree-spined

stickleback, Gasterosteus aculeatus L.

Journal of Fish Biology, vol. 10, pp. 467-472.

Studies on the

toxicity of cadmium to the three-spined

stickleback Gasterosteus aculeatus L. Journal

of Fish Biology, vol. 11, pp. 207-215.

Accumulation of

heavy metals in the whale worm Anisakis

simplex s.l (Nematoda: Anisakidae). Journal

of Marine Biology Association UK vol. 83,

pp. 905-906. Proteolytic

enzymes of Pomphorhynchus laevis and in

three other acanthocephalans. Journal of

Parasitology, vol. 80, pp. 45-49.

Cosmopolitan

bio-monitors of trace metals. Marine

Pollution Bulletin, vol. 26, pp. 593–601. The

growth, biomass, and fecundity of

Bothriocephalus acheilognathi in North

Carolina cooling reservoir. Journal of

Parasitology, vol. 73. pp. 893-900.

Methylmercury levels in a parasite

(Apophallus brevis metacercariae) and its

host, yellow perch (Perca flavescens).

Aquatic Ecology, vol. 42, pp. 495-501.

Cadmium accumulation in Moniliformis

moniliformis (Acanthocephala) from

experimentally infected rats. Parasitology

Research, vol. 86, pp. 688-691.

Neotrop. Helminthol., 3(2), 2009

107

Sures, B. 2003.

Siddall, R & Sures, B. 1998.

Smyth, JD. 1990.

Sures, B. 2001.

Sures, B. 2003.

Sures, B. 2004.

Sures, B. 2006.

Sures, B & Radszuweit, H. 2007.

Sures, B & Reimann, N. 2003.

Sures, B & Siddall, R. 1999.

Sures, B & Siddall, R. 2001.

Sures, B & Siddall, R. 2003.

Fish macroparasites as

indicators of heavy metal pollution in river

sites in Austria. Parasitology, vol. 123, pp.

S61-S69. Uptake of lead by

Pomphorhynchus laevis cystacanths in

Gammarus pulex and immature worms in

chub (Leuciscus cephalus). Parasitology

Research, vol. 84, pp. 573-577.

Acanthocephala. In (JD Smyth,

ed.). In vitro cultivation of parasitic

helminths. CRC Press, Boca Raton.

The use of fish parasites as

bioindicators of heavy metals in aquatic

systems: a review. Aquatic Ecology, vol. 35,

pp. 245-255.

Accumulation of heavy metals by

intestinal helminthes in fish: an overview and

perspective. Parasitology, vol. 126, pp. 53-

60. Environmental parasitology:

relevancy of parasites in monitoring

environmental pollution. Trends in

Parasitology, vol. 20, pp. 170-177.

How parasitism and pollution affect

the physiological homeostasis of aquatic

hosts. Journal of Helminthology, vol. 80, pp.

151-157. Pollution-induced

heat shock protein expression in the

amphipod Gammarus roeseli is affected by

lar vae of Polymorphus minutus

( A c a n t h o c e p h a l a ) . J o u r n a l o f

Helminthology, vol. 81, pp. 191-197.

Analysis of trace

metals in the Antarctic host-parasite system

Notothenia coriiceps and Aspersentis

megarhynchus (Acanthocephala) caught at

King George Island, South Shetland Islands.

Polar Biology, vol. 26, pp. 680-686.

Pomphorhynchus

laevis: the intestinal acanthocephalan as a

lead sink for its fish host, chub (Leuciscus

cephalus). Experimental Parasitology, vol.

93, pp. 66-72. Comparison between

lead accumulation of Pomphorhynchus

laevis (Palaeacanthocephala) in the intestine

of chub (Leuciscus cephalus) and in the body

cavity of goldfish (Carassius auratus auratus).

International Journal for Parasitology, vol.

31, pp. 669-673. Pomphorhynchus

laevis (Palaeacanthocephala) in the intestine

of chub (Leuciscus cephalus)as an indicator

of metal pollution. International Journal for

Parasitology, vol. 33, pp. 65-70. Cadmium

c o n c e n t r a t i o n s i n t w o a d u l t

acanthocephalans, Pomphorhynchus laevis

and Acanthocephalus lucii, as compared with

their fish hosts and cadmium and lead levels

in larvae of A. lucii as compared with their

crustacean host. Parasitology Research vol.

81, pp. 494-497.

Lead accumulation in Pomphorhynchus

laevis and its host. Journal of Parasitology,

vol. 80, pp. 355-357.

Comparative study of lead accumulation in

different organs of perch (Perca fluviatilis)

and its intestinal parasite, Acanthocephalus

lucii. Bulletin of Environmental

Contamination and Toxicology, vol. 52, pp.

269-273.

Lead content of Paratenuis ambiguus

(Acanthocephala), Anguillicola crassus

(Nematodes) and their host Anguilla

anguilla. Diseases of Aquatic Organisms, vol.

19, pp. 105-107.

Lead and cadmium content of two cestodes,

M o n o b o t h r i u m w a g n e r i a n d

Bothriocephalus scorpii, and their fish hosts.

Parasitology Research, vol. 83, pp. 618-623.

Intestinal fish parasites as heavy metal

bioindicators: a comparison between

A c a n t h o c e p h a l u s l u c i i

(Palaeacanthocephala) and the Zebra

mussel, Dreissena polymorpha. Bulletin of

Environment Contamination and Toxicology,

vol. 59 pp. 14-21.

Heavy metal concentrations in adult

acanthocephalans and cestodes compared to

their fish hosts and to established free-living

bioindicators. Parassitologia, vol. 39, pp.

213-218.

Relative concentrations of heavy metals in

the parasites Ascaris sum (Nematoda) and

Fasciola hepatica (Digenea) and their

respective porcine and bovine definitive

Sures, B & Taraschewski, H. 1995.

Sures, B, Taraschewski, H & Jackwerth. 1994a.

Sures, B, Taraschewski, H & Jackwerth. 1994b.

Sures, B, Taraschewski, H & Jackwerth. 1994c.

Sures, B, Taraschewski, H & Rokicki, J. 1997a.

Sures, B, Taraschewski, H & Rydlo, M, 1997b.

Sures, B, Taraschewski, H & Siddall, R. 1997c.

Sures, B, Jurges, G & Taraschewski, H. 1998.

Helminths as bioaccumulators of heavy metals de Buron et al.

108

hosts. International Journal for Parasitology,

vol. 28, pp. 1173-1178.

Parasites as accumulation indicators of

heavy metal pollution. Parasitology Today,

vol. 15, pp. 16-21.

Interaction between

cadmium exposure and infection with the

intestinal parasite Moniliformis

moniliformis (Acanthocephala) on the stress

hormone levels in rats. Environmental

Pollution, vol. 119, pp. 333-340. The

intestinal parasite Pomphorhynchus laevis

(Acanthocephala) interferes with the uptake

and accumulation of lead (210Pb) in its fish

host chub (Leuciscus cephalus). International

Journal for Parasitology, vol. 33, pp. 1617-

1622.

Lead concentrations in

Hymenolepis diminuta and Taenia

taeniaformis larvae compared to their rat

hosts (Rattus norvegicus)sampled from he

city of Cairo, Egypt. Parasitology, vol. 127,

pp. 483-487.

T h e

acanthocephalan Paratenuisentis ambiguus

as a sensitive indicator of the precious metals

Pt and Rh emitted from automobile catalytic

converters. Environmental Pollution,

vol.122, pp. 401-405.

Bioaccumulation of

selected trace elements in lung nematodes,

Pseudalius inflexus, of harbor porpoise

(Phocoena phocoena) in a Polish zone of the

Baltic Sea. The Science of the Total

Environment, vol. 220, pp. 19-24.

Host-parasite interactions

in Acanthocephala: a morphological

approach. Advances in Parasitology, vol. 46,

pp. 1-179. Comparative study on

the accumulation of heavy metals in different

organs of tench (Tinca tinca L. 1758) and

plerocercoids of its endoparasite Ligula

intestinalis. Parasitology Research, vol. 97,

pp. 156-159. Next

remarks to the knowledge of heavy metal

Sures, B, Siddall, R & Taraschewski, H. 1999.

Sures, B, Scheef, G, Klar, B, Kloas, W &

Taraschewski, H. 2002.

Sures, B, Dezfuli, BS & Krug, HF. 2003a.

Sures, B, Scheible, T, Bashtar, AR & Taraschewski,

H. 2003b.

Sures, B, Zimmerman, S, Stuben, C &

Ta r a s c h e w s k i , H . 2 0 0 3 c .

Szefer, P, Rokicki, J, Frelek, K, Skora, K &

Malinga, M. 1998.

Taraschewski, H. 2000.

Tekin-Ozan, S & Kir, I. 2005.

Tenora, F, Barus, V & Prokes M. 2002.

concentrations in gravid tapeworm species

parasitizing aquatic birds. Helminthologia,

vol. 39, pp. 143-148.

Heavy metal concentrations in

tapeworms Diploposthe laevis and

Microsomacanthus compressa parasitizing

aquatic birds. Helminthologia, vol. 38, pp.

63-66.

Concentrations of some heavy metals

in Ligula intestinalis plerocercoids (Cestoda)

and Philometra ovata (Nematoda) compared

to t h e ir ho s ts (O s tei c hthe y es) .

Helminthologia, vol. 37, pp. 15-18.

Parallel analysis of some

heavy metals concentrations in the

Anguillicola crassus (Nematoda) and the

European eel Anguilla Anguilla

(Osteichthyes). Helminthologia, vol. 36, pp.

79-81.

Concentration of heavy metals in perch

and its endoparasites in the polluted water

re se r vo ir i n E a s te r n S l o v ak i a.

Helminthologia, vol. 39, pp. 23-28.

Internal metal sequestration and its

ecotoxicological relevance: a review.

Environmental science & Technology, vol.

18, pp. 4705-4712. Heavy

metal levels in suspended sediments,

Crassostrea gigas, and the risk to humans.

Archives of Environmental Contamination

and Toxicology, vol. 55, pp. 442-450.

Metal pollution-induced

immunomodulation in fish. Annual Review

of Fish Diseases, vol. 3, pp. 305-325.

Population health risk due

to dietery intake of heavy metals in the

industrial area of Huludao city, China.

Science of the Total Environment, vol. 387,

pp. 96-104.

Experimental studies on lead

accumulation in the eel-specific

endoparasites Anguillicola crassus

(Nematoda) and Paratenuisentis ambiguous

(Acanthocephala) as compared with their

Tenora, F, Kracmar, S, Prokes, M, Barus & Sitko, J.

2001.

Tenora, F, Barus, V, Kracmar, S & Dvoracek, J.

2000.

Tenora, F, Barus, V, Kracmar, S, Dvoracek, J &

Srnkova J. 1999.

Turceková, L, Hanzelová, V & Spakulová, M.

2002.

Vijver MG, Van Gestel, CAM, Lanno, RP, Van

Straalen, NM & Peijnenburg, WJGM. 2004.

Widmeyer, JR & Bendell-Young, LI. 2008.

Zelikoff, JT. 1993.

Zheng, N, Wang, Q, Zhang, X, Zheng, D, zhang, Z

& Zhang S. 2007.

Zimmermann, S, Sures, B & Taraschewski, H.

1999.

Neotrop. Helminthol., 3(2), 2009

109

host, Anguilla anguilla. Archives of

Environmental Contamination and

Toxicology, vol. 37, pp. 190-195.

Accumulation of the precious metals

platinum, palladium and rhodium from

automobile catalytic converters in

Paratenuisentis ambiguus as compared with

its fish host, Anguilla Anguilla. Journal of

Helminthology, vol. 79, pp. 85-89.

Zimmermann, S, von Bohlen, A & Sures, B. 2005.

Correspondence to author/ Autor para correspondencia:

Isaure de Buron

Department of Biology College of

Charleston 58 Coming St. Charleston SC 29401. USA

E-mail:

deburoni@cofc.edu

Telefax: (843)–953-5343.

Telephone: (843)-953-5848

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