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Parasites and Pollutants: Effects of Multiple Stressors on Aquatic Organisms

June 2023
Environmental Toxicology and Chemistry 42(2)

DOI:10.1002/etc.5689

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Authors:

Daniel Grabner

University of Duisburg-Essen

Louisa Rothe

University of Duisburg-Essen

Bernd Sures

University of Duisburg-Essen

Parasites can affect their hosts in various ways, and this implies that parasites may act as additional biotic stressors in a multiple-stressor scenario, resembling conditions often found in the field if, for example, pollutants and parasites occur simultaneously. Therefore, parasites represent important modulators of host reactions in ecotoxicological studies when measuring the response of organisms to stressors such as pollutants. In the present article, we introduce the most important groups of parasites occurring in organisms commonly used in ecotoxicological studies ranging from laboratory to field investigations. After briefly explaining their life cycles, we focus on parasite stages affecting selected ecotoxicologically relevant target species belonging to crustaceans, molluscs, and fish. We included ecotoxicological studies that consider the combination of effects of parasites and pollutants on the respective model organism with respect to aquatic host-parasite systems. We show that parasites from different taxonomic groups (e.g. Microsporidia, Monogenea, Trematoda, Cestoda, Acanthocephala, Nematoda) clearly modulate the response to stressors in their hosts. The combined effects of environmental stressors and parasites can range from additive, antagonistic to synergistic. This review points to potential drawbacks of ecotoxicological tests if parasite infections of test organisms, especially from the field, remain undetected and unaddressed. If these parasites are not detected and quantified, their physiological effects on the host cannot be separated from the ecotoxicological effects. This may render this type of ecotoxicological test erroneous. In laboratory tests, for example to determine effect or lethal concentrations, the presence of a parasite can also have a direct effect on the concentrations to be determined and thus, on the subsequently determined security levels such as predicted no effect concentrations.

Life cycles of parasitic plathelminths. (A) Life cycle of monogenean. Adult parasites live on fish and reproduce. Eggs are released to the water and an Oncomiracidium hatches that actively locates a new fish host, attaches, and develops to the adult. (B) Macrodactylogyrus congolensis attached to the gill filament of Claris gariepinus (arrow). Scale bar 500 µm. (C) Opisthaptor of M. congolensis. Scale bar 200 µm (photographs in 3B and 3C by N. Smit). (D) Life cycle of the cestode Ligula intestinalis. Adult cestodes in the intestine of a fish-eating bird. Eggs are released with faeces from the bird and coracidium larva hatches in water. The coracidium is consumed by a copepod and develops in its hemocoel to the procercoid larva. A fish (second intermediate host) is consuming the infected copepod and the larva migrates to the body cavity, where it develops to the large plerocercoid larva. Birds get infected by feeding on infected fish containing the plerocercoids. The cestode larva matures in the bird intestine and adult worms reproduce sexually (Gutiérrez & Hoole, 2022). (E) Plerocercoid larva of L. intestinalis dissected from the body cavity of roach. (F) Generalized life cycle of Trematoda. Eggs are released by the definitive host. The next host (first intermediate host) is a mollusc, in most cases a snail, that gets infected by ingesting the parasite eggs or miracidia (the larval stage that hatches from eggs). In the snail, the parasite develops into sporocysts and/or rediae (depending on trematode species) and multiplies asexually. Large numbers of free-swimming larval stages (cercariae) are produced and released to the water where (depending on the trematode species) they infect a second intermediate host, encyst on plants or other organisms (e.g., shells of snails), or are directly infective for the final vertebrate host where the parasite reproduces sexually (Esch et al., 2002). (G) Cercaria of Echinostoma recurvatum. (H) Redia of E. recurvatum containing developing cercariae. Scale bars 100 µm. Photographs: J. Schwelm.

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(A) Life cycle of the acanthocephalan Pomphorhynchus sp. In the fish final host, the adult parasite lives in the intestine and reproduces sexually. The females lay eggs that are released with the host faeces and are infective for the intermediate host that takes up the eggs containing the acanthor stage orally (Taraschewski, 2000). In the amphipod intermediate host, the parasite develops to the acanthella and later to the cystacanth stage, which is trophically transmitted to the fish. (B) Infected amphipod with cystacanth larva in the body cavity that can grow to a considerable size compared with the host and is visible from the outside in the living host (arrow). (C) Opened fish intestine with heavy infection of Pomphorhynchus sp.

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Environmental Toxicology and Chemistry—Volume 00, Number 00—pp. 1–14, 2023

Received: 9 February 2023

Revised: 16 March 2023

Accepted: 4 June 2023 1

Environmental Toxicology

Parasites and Pollutants: Effects of Multiple Stressors

on Aquatic Organisms

Daniel Grabner,

* Louisa E. Rothe,

and Bernd Sures

a,b,c

Aquatic Ecology and Centre for Water and Environmental Research, University of Duisburg‐Essen, Essen, Germany

Research Center One Health Ruhr, Research Alliance Ruhr, University Duisburg‐Essen, Essen, Germany

Water Research Group, Unit for Environmental Sciences and Management, North‐West University, Potchefstroom, South Africa

Abstract: Parasites can affect their hosts in various ways, and this implies that parasites may act as additional biotic stressors

in a multiple‐stressor scenario, resembling conditions often found in the ﬁeld if, for example, pollutants and parasites occur

simultaneously. Therefore, parasites represent important modulators of host reactions in ecotoxicological studies when

measuring the response of organisms to stressors such as pollutants. In the present study, we introduce the most important

groups of parasites occurring in organisms commonly used in ecotoxicological studies ranging from laboratory to ﬁeld

investigations. After brieﬂy explaining their life cycles, we focus on parasite stages affecting selected ecotoxicologically

relevant target species belonging to crustaceans, molluscs, and ﬁsh. We included ecotoxicological studies that consider the

combination of effects of parasites and pollutants on the respective model organism with respect to aquatic host–parasite

systems. We show that parasites from different taxonomic groups (e.g., Microsporidia, Monogenea, Trematoda, Cestoda,

Acanthocephala, and Nematoda) clearly modulate the response to stressors in their hosts. The combined effects of envi-

ronmental stressors and parasites can range from additive, antagonistic to synergistic. Our study points to potential draw-

backs of ecotoxicological tests if parasite infections of test organisms, especially from the ﬁeld, remain undetected and

unaddressed. If these parasites are not detected and quantiﬁed, their physiological effects on the host cannot be separated

from the ecotoxicological effects. This may render this type of ecotoxicological test erroneous. In laboratory tests, for

example to determine effect or lethal concentrations, the presence of a parasite can also have a direct effect on

the concentrations to be determined and thus on the subsequently determined security levels, such as predicted no‐effect

published by Wiley Periodicals LLC on behalf of SETAC.

Keywords: Aquatic toxicology; Contaminants; Ecotoxicology; Environmental toxicology; Stressor

INTRODUCTION

In ecotoxicological studies, various test organisms are used

for either laboratory or ﬁeld investigations to assess the effects

of pollutants at various levels. In many cases, these test or-

ganisms might be infected by parasites. In fact, it is estimated

today that the number of parasite species ranges from one

third to over one half of the earth's total biodiversity

(Poulin, 2014; Poulin & Morand, 2004), therefore parasites are

common in most ﬁeld‐collected test organisms used to study

toxicant effects. Because parasites often act as an additional

stressor, they will likely affect the outcome of ecotoxicological

studies (Marcogliese & Pietrock, 2011; Sures et al., 2023; Sures,

Nachev, Selbach, et al., 2017). Adverse effects of parasites on

the health of their hosts can usually be expected given the fact

that they have long been recognized as important pathogens

of different organisms, among them humans and livestock

(Sures, Nachev, Pahl, et al., 2017). The harm associated with

parasites has long been the main reason to study parasites,

which ended up in a wealth of medical and veterinary text-

books about their pathogenic effects and their possible treat-

ment. Following this initial awareness of parasites several key

studies demonstrated the wide distribution of parasites in wild

animals and gave examples of their ecological implications and

effects on ecosystem processes (e.g., Hudson et al., 2006;

Poulin, 1999; Timi & Poulin, 2020; Tompkins et al., 2011; Wood

& Johnson, 2015). In this context, it has to be noted that effects

This is an open access article under the terms of the Creative Commons

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distribution in any medium, provided the original work is properly cited, the use is

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Published online 7 June 2023 in Wiley Online Library

(wileyonlinelibrary.com).

DOI: 10.1002/etc.5689

* Address correspondence to daniel.grabner@uni-due.de

are often more severe for intermediate hosts compared with

the ﬁnal host in the life cycle, particularly if the parasite is

trophically transmitted. Furthermore, some parasites do not

cause obvious effects on their hosts (Øverli & Johansen, 2019).

According to our common understanding, we can deﬁne a

parasite as an organism that lives in or on another organism of a

different species (host) and has some effect on the host that has

mostly a negative, but sometimes also a positive, effect on the

host ﬁtness (Bollache et al., 2002; Cornet et al., 2009; Giari

et al., 2020; Helluy, 2013; Jacquin et al., 2014; Marcogliese,

2004, 2005; Piscart et al., 2007; Sures, Nachev, Pahl, et al., 2017;

Thomas et al., 2000). Although this deﬁnition might also include

bacteria and viruses, the word “parasites”as opposed to

“pathogens”oftenrefersonlytoeukaryoticorganisms.Inthe

following sections, we use the term “parasite”in this sense.

Besides the consumption of host resources, parasites can mod-

ulate various host body functions such as the immune and hor-

mone system, metabolism and energy storage, the general stress

response (e.g., heat shock protein 70 [hsp70], cortisol), oxidative

stress, and other biomarkers (Ford & Fernandes, 2005; Marco-

gliese & Pietrock, 2011; Minguez et al., 2009; Morley, 2006;

Poulin, 1992; Sures, 2006, 2008a, 2008b; Sures, Nachev, Sel-

bach, et al., 2017; Tekmedash et al., 2016). In addition, several

parasites can accumulate toxicants and can reduce the tissue

concentrations in the host, which might, as a consequence, lead

to a different stress response in infected versus uninfected

hosts (Nachev & Sures, 2016; Sures & Nachev, 2022; Sures

et al., 2023). Before going into details with respect to possible

parasite–pollutant interactions and their combined effects on

hosts and ecotoxicologically relevant parameters, we will give a

brief overview of the most important groups of parasites occur-

ring regularly in selected ecotoxicological target species be-

longing to crustaceans, molluscs, and ﬁsh.

ECOTOXICOLOGICALLY RELEVANT

PARASITE TAXA

Some parasite groups occur frequently in test organisms

that are used in ecotoxicological studies and can have a sig-

niﬁcant impact on the response to further stressors. We brieﬂy

summarize the life cycles of the major parasite groups that are

relevant for our review.

Microsporidia

Taxonomically, the Microsporidia are closely related to the

fungi and belong to the group Opisthosporidia (Bojko

et al., 2022). They can parasitize a wide variety of hosts, in-

cluding crustacea and other invertebrates or ﬁsh, where they

develop intracellularly in various tissues, depending on the

microsporidian species. Transmission can be horizontally from

one host to the next or vertically via the gonads from mother to

offspring (Dunn et al., 2001; Smith, 2009; see Figure 1 for de-

tails). Because microsporidia cannot usually be detected by the

naked eye in their hosts, molecular analyses are necessary to

determine the infection status of the studied free‐living species

(e.g., Link et al., 2022).

Plathelminthes

The parasitic plathelminths comprise the Monogenea (skin

ﬂukes), Cestoda (tapeworms), and Trematoda (ﬂukes). Mono-

geneans are mostly ectoparasites (ﬂatworms of gills or skin) of

aquatic organisms like ﬁsh or amphibians (Figure 2A–C). They

have simple life cycles using a single host species and without

asexual reproduction (Figure 2A). Some species are oviparous,

(A)(B)

FIGURE 1: Life cycle of microsporidians with (A) horizontal and (B) vertical transmission. (A) Horizontally transmitted microsporidians are usually

more pathogenic, and development of spores leads to host death and release of spores to the environment, where they are taken up by uninfected

amphipods. (B) In the case of vertical transmission, stages of the parasite enter the eggs via the ovary of the female and are transmitted to the

offspring. Vertically transmitted microsporidians are dependent on the host reproduction and will not have a signiﬁcant impact on the survival of

their host (Dunn et al., 2001). Nevertheless, these parasites can modulate the sex ratio of their host population by either male killing or feminization

(e.g., amphipods; Haine et al., 2007; Smith, 2009; Stentiford & Dunn, 2014).

2Environmental Toxicology and Chemistry, 2023;00:1–14—Grabner et al.

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producing eggs that release a free‐swimming larval stage called

oncomiracidium, while some species are viviparous. On the host,

the adult monogeneans attach with a posterior structure, the

opisthaptor bearing hooks and/or suckers (Figure 2B,C), and

feed on mucus, epithelial cells, or blood (Bakke et al., 2007;

Buchmann & Bresciani, 2006). Monogenean populations were

found to react strongly to environmental stressors like metals or

eutrophication (Gilbert & Avenant‐Oldewage, 2021) and were

(A)(D)

(E)

(B)

(F)

(G)

(H)

(C)

FIGURE 2: Life cycles of parasitic plathelminths. (A) Life cycle of monogenean. Adult parasites live on ﬁsh and reproduce. Eggs are released to the

water and an Oncomiracidium hatches that actively locates a new ﬁsh host, attaches, and develops to the adult. (B)Macrodactylogyrus congolensis

attached to the gill ﬁlament of Claris gariepinus (arrow). Scale bar 500 µm. (C) Opisthaptor of M. congolensis. Scale bar 200 µm (photographs in 3B

and 3C by N. Smit). (D) Life cycle of the cestode Ligula intestinalis. Adult cestodes in the intestine of a ﬁsh‐eating bird. Eggs are released with faeces

from the bird and coracidium larva hatches in water. The coracidium is consumed by a copepod and develops in its hemocoel to the procercoid

larva. A ﬁsh (second intermediate host) is consuming the infected copepod and the larva migrates to the body cavity, where it develops to the large

plerocercoid larva. Birds get infected by feeding on infected ﬁsh containing the plerocercoids. The cestode larva matures in the bird intestine and

adult worms reproduce sexually (Gutiérrez & Hoole, 2022). (E) Plerocercoid larva of L. intestinalis dissected from the body cavity of roach.

(F) Generalized life cycle of Trematoda. Eggs are released by the deﬁnitive host. The next host (ﬁrst intermediate host) is a mollusc, in most cases a

snail, that gets infected by ingesting the parasite eggs or miracidia (the larval stage that hatches from eggs). In the snail, the parasite develops into

sporocysts and/or rediae (depending on trematode species) and multiplies asexually. Large numbers of free‐swimming larval stages (cercariae) are

produced and released to the water where (depending on the trematode species) they infect a second intermediate host, encyst on plants or other

organisms (e.g., shells of snails), or are directly infective for the ﬁnal vertebrate host where the parasite reproduces sexually (Esch et al., 2002).

(G) Cercaria of Echinostoma recurvatum.(H) Redia of E. recurvatum containing developing cercariae. Scale bars 100 µm. Photographs: J. Schwelm.

Parasites and pollutants—Environmental Toxicology and Chemistry, 2023;00:1–14 3

found to respond to environmental pollution (Sanchez‐Ramirez

et al., 2007).

In contrast to monogeneans, adult cestodes (tapeworms)

live in the host intestine. These parasites can have complex

life cycles with details that can vary largely depending on

the cestode species (Figure 2D,E). For example, the cestode

Ligula intestinalis, a parasite that interfers with the hormone

balance of its ﬁsh intermediate host, has a life cycle including a

copepod, a ﬁsh intermediate host, and a bird as the ﬁnal

host (Figure 2D). L. intestinalis has a strong inﬂuence on the

hormone system of the ﬁsh and thereby interferes with host

reproduction (Schabuss et al., 2005; Trubiroha et al., 2010).

The life cycles of trematodes involve a vertebrate ﬁnal

host and one or two intermediate hosts, including a phase of

massive asexual multiplication in the ﬁrst intermediate host

(mostly snail; see Figure 2F–H for details).

Acanthocephala

The exclusively parasitic helminth group Acanthocephala is

also called “thorny‐headed worms.”These parasites have life

cycles that involve an invertebrate intermediate host (e.g., am-

phipods) and a vertebrate ﬁnal host (e.g., ﬁsh; Kennedy, 2006;

Perrot‐Minnot et al., 2023; see Figure 3 for details). The cys-

tacanth larvae (Figure 3B) often manipulate the behaviour of

their invertebrate intermediate host by interfering with host

physiology to enhance the trophic transmission to the ﬁnal host

(Helluy, 2013) and thereby execute a variety of physiological

effects (e.g., Bailly et al., 2018; Bakker et al., 2017; Bollache

et al., 2000; Cornet, 2011), which might also be important for

ecotoxicological studies (Grabner & Sures, 2019). Adult acan-

thocephalans (Figure 3C) are known to accumulate enormous

amounts of metals inside their bodies, often exceeding the

concentrations detected in the organs of their ﬁsh hosts (Sures &

Nachev, 2022). This enormous metal accumulation might even

lead to reduced metal concentrations in tissues of infected hosts

as compared with uninfected ones (see Sures, Nachev, Selbach,

et al., 2017; Sures et al., 2023, and references therein), sug-

gesting that adult acanthocephalans might be beneﬁcial to their

hosts under polluted conditions.

Nematoda

Not many nematodes (also called roundworms) have been

studied in an ecotoxicological context so far. One species for

which additional stressor effects on the host are comparatively

well studied is the eel nematode Anguillicola crassus. This

parasite is an invasive eel parasite in Europe and other parts

of the world, and uses different species of copepods as

intermediate hosts (see Figure 4 for details). As adults, these

nematodes suck blood from the capillaries inside the swim

bladder of eels and are therefore considered a serious threat to

the population of European eels (Sures & Knopf, 2004).

PARASITES AND POLLUTANTS AS

MULTIPLE STRESSORS

When parasitized test organisms are exposed to additional

stressors such as pollutants, they are subjected to multiple

stressors (Sures et al., 2023). The effects of the combined

stressors might be different compared with what can be

expected from each single stressor. Conceptually, there can be

different scenarios when dealing with two stressors (Figure 5):

First, one of the stressors can be dominant and override

(A)(B)

(C)

FIGURE 3: (A) Life cycle of the acanthocephalan Pomphorhynchus sp. In the ﬁsh ﬁnal host, the adult parasite lives in the intestine and reproduces

sexually. The females lay eggs that are released with the host faeces and are infective for the intermediate host that takes up the eggs containing

the acanthor stage orally (Taraschewski, 2000). In the amphipod intermediate host, the parasite develops to the acanthella and later to the

cystacanth stage, which is trophically transmitted to the ﬁsh. (B) Infected amphipod with cystacanth larva in the body cavity that can grow to a

considerable size compared with the host and is visible from the outside in the living host (arrow). (C) Opened ﬁsh intestine with heavy infection of

Pomphorhynchus sp.

4Environmental Toxicology and Chemistry, 2023;00:1–14—Grabner et al.

the effects of the second stressor. Second, the two stressors

do not inﬂuence each other in a way that their combined

effect is additive and, third, there can be an interaction be-

tween the stressors that is either synergistic or antagonistic

(Birk et al., 2020). In addition, there can be special cases, for

example the reversal of the response to combined stressors

compared with the predicted effect (Jackson et al., 2016; Vos

et al., 2023).

In the present study, we summarized examples that illustrate

the combined effects of parasites and pollutants on the

response of the host, focusing on aquatic parasites. Examples

that refer to the mere effects of the parasite are not considered

here. Also, we are not addressing studies describing the

effects of stressors on the parasite population or community.

Furthermore, we want to highlight some ﬁelds of research that

should be addressed to improve our understanding of the role

of parasites in ecotoxicological research. Overall, we intend to

create awareness in the ecotoxicology community for the wide

variety of effects parasites might have alone or in combination

with other stressors on the physiological homeostasis of their

hosts in ﬁeld and experimental studies. Moreover, when

addressing regulatory issues with the aim of determining safe

environmental contaminant concentrations, such approaches

should also consider parasitised test organisms because

(B)(A)

FIGURE 4: Life cycle of the eel nematode Anguillicola crassus.(A) Life cycle including the eel ﬁnal host where the adult nematodes live in the swim

bladder and reproduce sexually. Eggs are released with eel faeces and the L2 larval stage is taken up by copepods. The larva moults to the L3 stage,

which is infective for the eel (De Charleroy et al., 1990). Optional paratenic ﬁsh hosts can feed on infected copepods and transmit the parasite to

eels (Moravec & Skorikova, 1998; Thomas & Ollevier, 1992). (B) Photograph of A. crassus adults recovered from a dissected swim bladder.

FIGURE 5: Schematic overview of the effects of parasitism and pollution‐related stress on organisms at various levels. Potential response is shown:

(a) additive effect of both stressors, (b) antagonistic effect, and (c) synergistic effect. Black arrows, effect of individual stressor; green arrows,

combined effect of both stressors; +/−indicates direction of effect). Some elements of the ﬁgure were created with BioRender.com.

Parasites and pollutants—Environmental Toxicology and Chemistry, 2023;00:1–14 5

parasites could alter both contaminant accumulation patterns

and host responses to contaminants.

COMBINED EFFECTS OF PARASITES AND

OTHER STRESSORS

In this section, we give examples of the response of

organisms to both parasites and other (mostly chemical)

stressors. The examples are grouped by the way of stressor

interactions (additive, synergistic, antagonistic) as far as this can

be inferred from the results. Finally, we will address several

further aspects that determine the interaction of parasites and

other stressors.

Putative additive effects

An additive effect occurs if the measured response of a test

organism to a chemical stressor is further increased due to in-

fection by a parasite. There are not many examples that could

be recovered from the literature describing an additive effect of

parasite +stressor. This might indicate that the interaction of

parasites and additional stressors shows a more complex pattern

in most cases. One example of a signiﬁcant additive effect on

mortality was found for sockeye salmon (Oncorhynchus nerka)

that were exposed to zinc if in addition they were

infected with adult cestodes (Eubothrium salvelini). The time

to reach 50% mortality was reduced by 25% in infected and

exposed ﬁsh relative to uninfected and exposed ﬁsh (Boyce &

Yamada, 1977). Similarly, individuals of three‐spined sticklebacks

(Gasterosteus aculeatus) infected with plerocercoid larvae of the

cestode Schistocephalus solidus showed increased mortality

(maximum reduction of mean period of survival from ~800 to

300 h) and consequently a lower 50% lethal concentration (LC50)

for cadmium compared with uninfected ﬁsh (Pascoe &

Cram, 1977). On the sublethal level, an additive effect of para-

site and pollution on the number of pigmented macrophages

was observed in spottail shiners (Notropis hudsonius)infectedby

the apicomplexan Eimeria degiustii (Thilakaratne et al., 2007).

Additive effects were also detected for ectoparasites and pol-

lution exposure. In the guppy Poecila reticulata,exposuretozinc

led to increased epidermal thickness, and infection with the

monogenean Gyrodactylus turnbulli further increased this effect

at moderate parasite densities (Gheorghiu et al., 2012). A similar

additive effect was found for the activities of the biomarkers

aspartate aminotransferase and alanine aminotransferase, and

the concentrations of creatinine and urea in ﬁsh (Oreochromis

niloticus,Clarias gariepinus) exposed to elevated metal levels

and ectoparasites (Monogenea, Crustacea, Protozoa). The bio-

marker levels in infected ﬁsh were increased by 13% to 40%

compared with uninfected ﬁsh (El‐Seify et al., 2011).

These examples show that the lack of consideration of

parasite infections can lead to an overestimation of the toxicity

of a pollutant according to the effects on the host. On the other

hand, results obtained from parasite‐free populations can lead

to false conclusions about the toxic potential of a substance

under ﬁeld conditions when parasites come into play.

Putative synergistic effects

In contrast to the simple additive effect of two stressors,

synergistic effects might lead to unexpected results that cannot

be predicted based on the single stressor effects. In some

cases, the effects of toxicants only become detectable in par-

asitized hosts (Coors & De Meester, 2008; Coors et al., 2008;

Rothe et al., 2022). Furthermore, toxicant effects can be in-

creased by the parasite to a higher level than expected based

on the outcome of each single stressor exposure (either pol-

lution or parasite) due to a synergistic effect of the two stressors

(Thilakaratne et al., 2007). As a consequence, the combined

effect of parasites and pollution is higher than the sum of the

two effects measured in a single exposure, thus parasites can

make pollution effects detectable, which may result in a pol-

lutant being deemed environmentally relevant. Conversely, the

effects of parasites can become apparent through additional

exposure of the host to further stressors. For example, a dif-

ferential response of the biomarker lipid peroxidation (~26%

higher in infected ﬁsh) between individuals of yellow perch

(Perca ﬂavescens) that were infected or uninfected with the

nematode Raphidascaris acus was only observed if an addi-

tional chemical stressor was present (Marcogliese, Brambilla,

et al., 2005). A comparable reaction was found in female

Gammarus roeselii that were exposed to cadmium and infected

with microsporidian parasites. The amphipods showed reduced

energy reserves (~40% decrease in total lipids and 30% de-

crease in glycogen level relative to the uninfected amphipods),

elevated susceptibility to oxidative stress (up to 60% decreased

levels of reduced glutathione relative to uninfected amphi-

pods) and approximately 50% increased cellular damage

(based on levels of malondialdehyde) compared with unin-

fected cadmium‐exposed individuals. Parasite infection alone

did not affect the tested biomarkers (Gismondi et al., 2012b).

Presumably, the change in host metabolism caused by the

parasite leads to a stronger response to another stressor. This

in turn illustrates that a parasitized population may already

show effects at lower pollutant concentrations than would be

the case with a non‐parasitized population.

Putative antagonistic effects

In some cases, parasites increase the tolerance of the host

to stressors due to an antagonistic effect of the parasite. In this

context, Piscart et al. (2007) found that acanthocephalan‐

infected amphipods show an increased tolerance to elevated

salinity levels of approximatley 60% to more than 100% based

on LC50. Similarly, cestode larvae were described to increase

Artemia sp. resistance to arsenic during acute toxicity tests

(Sánchez et al., 2016). In infected Artemia sp., consistently in-

creased LC50 values (50% to over 100%) were found compared

with uninfected conspeciﬁcs. Even after increasing the water

temperature from 25 °C to 29 °C the beneﬁcial effects of the

cestode infection prevail with infected Artemia sp. The latter

showed approximately 60% higher levels of catalase and

approximately 50% higher glutathione reductase activity

compared with uninfected individuals, which both can be

6Environmental Toxicology and Chemistry, 2023;00:1–14—Grabner et al.

interpreted as protection measures against (temperature‐

induced) oxidative stress (Sánchez et al., 2016).

Likewise, a positive effect on survival of infected compared

with uninfected hosts was found in some cases for trematode‐

infected snails (Zeacumantus subcarinatus) that were exposed

experimentally to different ocean‐acidiﬁcation conditions. At

pH 7.6, mortality ranged between 3% and 23% in infected

snails (depending on the trematode species) and was 28% in

uninfected snails. At pH 7.4, the mortality rate of infected snails

ranged from 13% to 31% compared with 22% for the unin-

fected snails. In contrast at pH 8.1, the mortality rate of unin-

fected snails was lower (3%) compared with infected snails

(7%–33%; MacLeod & Poulin, 2016b). A similar ﬁnding was

made for trematode‐infected mussels (Pisidium amnicum) ex-

posed to pentacholorophenol. The mean survival time of the

infected mussels was increased by more than 100% at 19 °C

but there was an overall negative ﬁtness effect of the parasite

due to castration of the host (Heinonen et al., 2001). Reduced

mortality of the host even under stressor exposure might be

beneﬁcial for the parasite because the host will provide habitat

and resources for growth, development, and/or multiplication

of the parasite (e.g., trematode larvae in snails). Even for

trophically transmitted parasites (e.g., cestode larvae in

Artemia sp.) survival of the intermediate host is essential during

the development of the parasite larva (until it is infective for the

next host; see Bailly et al., 2018; Dianne et al., 2011; Franceschi

et al., 2008). Furthermore, host death might interfere with

transmission if the ﬁnal host feeds only on live prey.

Another example of a potential protective effect of acan-

thocephalans was found in chub (Squalius cephalus), where

signiﬁcantly lower oxidative damage was observed in tissues of

chub that were exposed to organic pollutants if they were also

infected with acanthocephalans (Pomphorhynchus sp.; Molbert

et al., 2020). In general, some acanthocephalan species are

presumably beneﬁcial for their host because there are several

studies showing the accumulation potential of acanthocepha-

lans for metals. Tissue concentrations of metals in the parasite

can highly exceed those of the host and metal concentrations

can even be reduced in tissues of infected compared with

uninfected hosts (Sures, 2006; Sures, Nachev, Selbach,

et al., 2017; Sures et al., 2023).

Antagonistic effects of parasites can also have negative

consequences for the host if a protective stressor response

(e.g., hsp70, metallothioneins) is decreased in infected hosts.

Such a case was found in cockles (Cerastoderma edule) in-

fected by trematodes and exposed to cadmium. By reducing

the production of protective metallothioneins by 70% relative

to the uninfected hosts, the parasites impaired the detox-

iﬁcation mechanisms of the host and caused an increase in

cadmium accumulation (795 ng/g in infected vs. 569 ng/gin

uninfected cockles) and presumably increased toxic effects

(Baudrimont & de Montaudouin, 2007). The larvae of the

acanthocephalan parasite Polymorphus minutus reduced

(~80% compared with uninfected amphipods) or completely

disrupted the hsp70 response caused by cadmium or heat

exposure in amphipods (Gammarus fossarum and G. roeselii;

Frank et al., 2013; Sures & Radszuweit, 2007). It is not clear to

date whether the reduction of the detoxiﬁcation capabilities or

the cellular defence mechanisms have an effect on host ﬁtness.

Also, the potential biological signiﬁcance of the impairment for

the parasite is not known.

Another presumably antagonistic effect of the combination

of parasite and chemical stress was observed in a study of

European eel (Anguilla anguilla) infected with the swim‐bladder

nematode Anguillicola crassus that were exposed to both

cadmium and 3,3′,4,4′,5‐pentachlorobiphenyl (PCB 126). At the

end of the experiment, cortisol levels in the parasite‐infected

and chemical‐exposed group were only 60% of those of the

parasitized eel without exposure. An explanation could be

cortisol‐mediated immune suppression induced by the parasite

that might be disturbed by the chemical exposure (Sures

et al., 2006). However, it is not known whether the interference

with immune suppressive mechanisms of the parasite inﬂu-

ences the host defence against the parasite.

No combined stressor effects

It is important to note that parasites do not necessarily have

an inﬂuence on the effects of further stressors in the host. For

example, no effect of parasitism on the host response was

found in toxaphene‐exposed Arctic charr (Salvelinus alpinus)

infected with the tapeworm Diphyllobothrium dendriticum and

tadpoles of the frog Rana palustris exposed to malathion and

infected with the trematode Echinostoma trivolvis (Blanar

et al., 2005; Budischak et al., 2009). Similarly, parasites had no

signiﬁcant effect on the biomarker response of common carp

(Cyprinus carpio) and African sharptooth catﬁsh (Clarias

gariepinus) sampled from stream sites with elevated metal

concentrations in the study of Erasmus et al. (2020), even

though several metals were accumulated by the parasites and

thereby reduced in the host tissues. These examples show that

it is not possible to assume in all cases that parasites will affect

the response of the host to pollutants. Nevertheless, the host

stress response in relation to parasites can be affected by fur-

ther factors, for example the infection intensity of the parasite

(see section Additional factors inﬂuencing the host stress

response).

Additional factors inﬂuencing the host stress

response

The effect of parasites on the host response to other stres-

sors is difﬁcult to generalize because the outcome can be de-

pendent on a variety of factors, some of which are outlined in

this section.

Temperature. When using temperature as a stressor it was

found that infection by the trematode Himasthla elongata in-

creased the mortality of the gastropod host Littorina littorea at

elevated temperatures (e.g., median survival duration of 5 and

16 days for infected and uninfected snails, respectively; Diaz‐

Morales et al., 2022). In a similar way, brown trout (Salmo trutta)

fry and alevins exposed to the oomycete Saprolegnia parasitica

Parasites and pollutants—Environmental Toxicology and Chemistry, 2023;00:1–14 7

showed increased mortality in the parasite treatment (50% up

to 100% mortality compared with <30% in the uninfected ﬁsh)

when facing intermittent temperature increases (Casas‐Mulet

et al., 2021). Temperature is normally controlled in laboratory

experiments and reported in ﬁeld studies. However, when

planning studies, especially with parasites, it must be consid-

ered that different temperature levels can lead to signiﬁcantly

different results. There are several other examples where bio-

marker responses due to parasites and additional stressors

showed additive, but overall complex patterns (e.g., con-

trasting results depending on host sex). These studies will be

shown in the following sections.

Species‐speciﬁc effects. Effects of stressors were found to be

highly species‐speciﬁc depending on the parasite and host

species studied, with clear differences found even for closely

related taxa. For example, exposure to desethylatrazine caused

an increase in mortality in the freshwater gastropod Stagnicola

elodes if infected by a trematode (gymnocephalus‐type cer-

cariae, ~30% survival) but did not affect mortality in exposed

snails infected with Echinoparyphium sp. (~80% survival;

Koprivnikar & Walker, 2011). Parasite species also made a con-

siderable difference in the study of MacLeod and Poulin (2016a),

who found signiﬁcantly variable rates of oxygen consumption

and tissue glucose levels in the intertidal gastropod Z. sub-

carinatus kept at different pH treatments depending on the

trematode species present. Similarly, the reaction of the stress

protein hsp70 can be modulated by parasites, but the outcome

depends largely on the host–parasite system studied. While

elevated temperature or cadmium exposure in combination with

microsporidian infection caused increased hsp70 levels in Gam-

marus pulex and G. fossarum, there was no modulation of hsp70

by the acanthocephalan P. minutus in G. fossarum, irrespective of

the exposure (Chen et al., 2015; Grabner et al., 2014). On the

other hand, an over 2000% higher induction of hsp70 was found

in the study of Frank et al. (2013) in P. minutus‐infected G. fos-

sarum. In the same study, cadmium exposure also induced a

more than 7000% increase of hsp70 levels, whereas the combi-

nation of parasite and cadmium resulted in a lower hsp70 re-

sponse than the metal exposure in uninfected individuals (Frank

et al., 2013). These partly contradictory results might be due to

unnoticed microsporidian infections in the amphipods in the

study of Frank et al. (2013). Rothe et al. (2022) found an in-

creasing effect on several biomarkers in the same P. minutus–G.

fossarum system, whereas there was no signiﬁcant effect of

treated wastewater. Interestingly, the same acanthocephalan

species completely disrupted the hsp70 response of the am-

phipod G. roeselii even after exposure to palladium and heat

(Sures & Radszuweit, 2007). The impairment of the stress re-

sponse by one parasite‐pollutant combination can be further

modulated by coinfecting parasites present in the same host

individual. For example, microsporidian parasites can disrupt the

effects of acanthocephalan parasites on the host. In G. roeselii

infected with both the microsporidian Dictyocoela roeselum and

the acanthocephalan P. minutus, the microsporidian effects on

the biomarker response dominated that of the acanthocephalan

compared with infections with only a single parasite (Gismondi

et al., 2012a). The reason for this observation might be the more

severe impact of the microsporidians on host metabolism during

phases of massive multiplication.

These examples make it clear that it is not appropriate to

speak of parasites in general terms if we want to understand

ecotoxicological relationships. On the contrary, different par-

asite taxa need to be considered individually and their impact

on the host has to be assessed in each case.

Concentration‐dependent or parasite infection intensity

effects. It was found that the effects of parasites can vary

greatly depending on the concentration of the pollutants or the

number of parasite stages per host. For example, trematodes

in ﬁsh (yellow perch, P. ﬂavescens) caused an increase in cat-

alase and a decrease of glutathione reductase activity but only

at sites with the highest pollutant levels, while no parasite

effect on the biomarker response was observed in ﬁsh from

sites with low pollutant concentrations (Marcogliese

et al., 2010). Molbert et al. (2021) also found a response of

chub (S. cephalus) parasitized with acanthocephalans (Pom-

phorhynchus sp.) depending on the exposure levels to poly-

cyclic aromatic hydrocarbons (PAHs). Interestingly, levels of

oxidative stress were more than 60% higher in parasitized ﬁsh

exposed to low PAH levels but approximately 40% lower at

higher PAH concentrations compared with uninfected ﬁsh from

the same exposure. Similarly, northern leopard frogs (Lith-

obates pipiens) naturally exposed to different atrazine levels

showed an interaction of the nematode parasite Oswaldocruzia

sp. and atrazine on the oxidative stress marker thiol. Thiol levels

were increased with parasite abundance, but only at low atra-

zine levels while decreasing thiol levels were measured

with increasing parasite abundance at high atrazine levels

(Marcogliese et al., 2021). An effect of infection intensity was

found in yellow perch (P. ﬂavescens) infected with trematode

metacercariae of the trematode A. brevis. If more than

10 metacercariae were detected, the ﬁsh showed 40% to

50% higher levels of lipid peroxidation than ﬁsh with <10

metacercariae (Marcogliese, Brambilla, et al., 2005).

Overall, these results show that the stress response of the

host often is not linearly related to parasite intensity and/or

pollutant concentrations, therefore it is important to test a

range of pollutants, but at the same time to consider parasite

infection intensity for the effect that is caused in the host. In-

fection intensity is not always considered, mainly for micro-

parasites that cannot be quantiﬁed easily. For parasite stages

that are not directly countable, semiquantitative methods

could be applied (e.g., rating intensity from low, medium to

high), or molecular methods such as quantitative polymerase

chain reaction could be used.

Effect of host age. The age distribution in the host pop-

ulation plays an important role to determine infection param-

eters and disease progression (Ben‐Ami, 2019; Thomas, 2002).

This aspect has been rarely investigated in an ecotoxicological

context. For example, Thilakaratne et al. (2007) found stronger

parasite‐induced effects according to the biomarker response

in younger spottail shiners (N. hudsonius) compared with older

8Environmental Toxicology and Chemistry, 2023;00:1–14—Grabner et al.

ﬁsh. In many cases it will be difﬁcult to determine the age of

the hosts if no laboratory‐bred individuals are available. Host

size can be used for some species for an approximation of host

age or at least to distinguish juvenile from adult individuals.

Effect of host gender. Gender is also an important factor

that can have a tremendous effect on the outcome of eco-

toxicological studies, as has been shown, for example, for

amphipods (Gismondi et al., 2013). Accordingly, the response

to the combined effects of parasites and further stressors is

often dependent on the host sex. Minguez et al. (2009) found

structural changes in the lysosomal system and an increase in

neutral lipids in the tissues of male Dreissena polymorpha

infected with parasites and exposed to pollution (30% higher

males), whereas the opposite trend was found in parasitized

and exposed female D. polymorpha (45% higher in females).

In an amphipod–acanthocephalan system, under cadmium

exposures, decreased mortality was found for G. roeselii

males infected with P. minutus compared with uninfected

amphipods (LC50 almost 200% higher in infected amphi-

pods). In contrast, mortality was increased (LC50 more than

200% higher in uninfected amphipods), and a stronger re-

sponse of toxic effect biomarkers was found in infected and

exposed females compared with uninfected individuals (e.g.,

50% increased malondialdehyde levels in cadmium‐exposed

uninfected females, whereas infected females showed an in-

crease of 160% under cadmium exposure; Gismondi, Beisel,

et al., 2012; Gismondi, Cossu‐Leguille, et al., 2012). Similarly,

glycogen levels were increased by 60% only in female

G. fossarum infected with the microsporidian Dictyocoela

duebenum and exposed to sublethal cadmium levels, but not

in males, in the study of Chen et al. (2015). Complex sex‐

speciﬁc differences were also found in the marine amphipod

Gammarus tigrinus exposed to different temperature levels

and infected with the trematode Podocotyle atomon.Infected

females showed lower phenoloxidase activity than males at

14 and 18 °C, and catalase activity was increased at higher

temperatures for infected males and uninfected females while

being increased at lower temperatures for infected females

(Diaz‐Morales et al., 2023).

These results highlight that host sex should be used as a

factor in the analysis of stressor effects. Furthermore, it is

important to improve the understanding of differences in the

reaction of female and male individuals to pollutants and par-

asites, and to clarify the underlying mechanisms.

FUTURE DIRCTIONS OF RESEARCH ON

PARASITES AND STRESSORS

The examples presented in the previous section (Com-

bined effects of parasites and other stressors) illustrate the

inﬂuence of parasites on the stress response of the host and

therefore their importance for ecotoxicological studies. We

therefore advocate the deliberate inclusion of parasite in-

fectionintheplanninganddesign of ecotoxicological studies.

The possible forms of interaction of the effects (additive,

synergistic, antagonistic) should be taken into account when

formulating hypotheses. Furthermore, based on the addi-

tional factors inﬂuencing parasite/stressor interactions out-

lined above, we recommend that the following factors, which

have received little attention to date, should be considered to

a greater extent. First, different temperature and pollutant

levels should be applied to study the gradient of responses of

both parasitized and unparasitized hosts. If possible, parasite

infection intensities should be assessed, or even controlled.

Second, host age and gender should be assessed and used as

factors whenever possible. This will improve the systematic

investigation of parasite effects, including additional stressors,

and lead to a mechanistic understanding of how parasites

inﬂuence the host response.

Furthermore, there are some elements of the host biology

that can be inﬂuenced both by environmental stressors and

parasites, but their interaction is only poorly understood: en-

docrine effects of parasites and pollutants, and the interactive

effects of parasites and chemical stressors on the host micro-

biome. Due to their importance for ecotoxicological questions,

both aspects will be summarized brieﬂy in the following sec-

tions. In addition, there are common test organisms that have

not been subject to studies involving parasites, although they

can be affected by various parasites in natural systems.

Effects of parasites on the endocrine system

of the host

Some parasites interfere with the endocrine system of their

host, mostly impairing the reproductive system or causing the

phenomenon of intersex, for example the cestode larva of

Ligula intestinalis in ﬁsh, trematodes in snails, or vertically

transmitted (from mother to offspring) microsporidians (Ford

& Fernandes, 2005; Grabner & Sures, 2019; Jobling &

Tyler, 2003; Lewis et al., 2015; Morley, 2006; Trubiroha

et al., 2009). Pollution might have similar effects that can be

difﬁcult to disentangle from the parasite (Ford et al., 2006;

Schabuss et al., 2005; Yang et al., 2008). For example, in the

amphipod G. pulex it was found that vertically transmitted

microsporidian parasites interfere with the effects of the en-

docrine disruptor cyproterone on sperm production of the

host (Gismondi et al., 2017).

Further studies are needed to understand the combined

effect on the endocrine system of parasites and chemicals, for

example those enhancing the knowledge of relevant bio-

markers to assess feminization or sexual dysfunction and dis-

tinguish between the effects of parasites and toxicant exposure

(Short et al., 2014). As a starting point, relatively well‐studied

endocrine‐disrupting parasites, for example L. intestinalis as a

model parasite in vertebrates and microsporidians in amphi-

pods for invertebrates, should be studied in more detail.

However, for the latter, much more fundamental knowledge

needs to be gained on the endocrine‐disrupting effects of the

parasite itself. The goal should be to analyse the combination

of parasites that affect the hormone system of the host with

exposure to endocrine‐disrupting chemicals.

Parasites and pollutants—Environmental Toxicology and Chemistry, 2023;00:1–14 9

Effects of the host microbiome

Studying the role of the microbiome of organisms is be-

coming more and more important in various research ﬁelds.

This applies also to ecotoxicology, where the interplay of the

gut microbiota, toxicant exposure, and physiological effects is

being investigated (Claus et al., 2016). Recent ﬁndings high-

light that parasites have a substantial inﬂuence on the host

microbiome (Dheilly et al., 2019; Fu et al., 2022) and that the

effects of parasites on the gut microbiota of ﬁsh (chub, Squalius

cephalus) can be more pronounced than exposure to PAHs

(Colin et al., 2022). Nevertheless, this research ﬁeld is in its

infancy and the signiﬁcance of changes in the microbiome

(e.g., by parasites and/or pollutants) for the host is still un-

known, therefore the ﬁrst step is to improve knowledge of the

microbiome function in vertebrates and invertebrates. The

second step is to test of the microbiome response to parasite

and pollutant exposure. Exposure‐related changes in the host

microbiome might also provide explanations for stressor effects

reported previously (e.g., biomarker responses).

Further parasites and pathogens that might have

an inﬂuence on the stress response

The parasites of some commonly used test organisms have

been well characterized and we already have some knowledge of

the combined effects of toxicant exposure, for example for

amphipods, ﬁsh, snails, and mussels (see above). Daphnia spp.

can be affected by a number of parasites under natural con-

ditions (Stirnadel & Ebert, 1997) and provide a great opportunity

to study parasite (e.g., Microsporidia) and environmental stressor

effects under laboratory conditions because protocols exist

for the controlled infection of Daphnia under these conditions

(e.g., Coors et al., 2008). However, there is a number of common

ecotoxicological test organisms for which only limited in-

formation is available on the role of parasites in addition to other

stressors. Zebraﬁsh, for example, can be affected by several

parasite taxa even under laboratory conditions (Kent et al., 2020)

and infections by microsporidians were even found in research

strains with sometimes subclinical infections that might affect

the outcome of experiments (Sanders et al., 2012). Among

invertebrate models, the nematode Caenorhabditis elegans is

used in ecotoxicological standard tests (e.g., Schertzinger

et al., 2017), but free‐living individuals can be infected by

microsporidians or pathogenic bacteria (Hodgkin & Partridge,

2008), therefore toxicity testing including parasitized test groups

might be possible for this species. Lubriculus variegatus is

also commonly used for ecotoxicological sediment testing

(e.g., Kontchou et al., 2023), but Lumbriculus spp. (and other

oligochaetes) are also common hosts for myxozoans (Kent et al.,

2001). This might be an interesting host–parasite model because

infected individuals can be identiﬁed according to the detection

of actinospores from infected individuals.

Some of the test organisms are available as pathogen‐free

cultures, for example C. elegans,Lumbriculus spp., and Daphnia

sp., and provide the possibility to study toxicant effects

without confounding effects from parasites. However, from an

ecotoxicological perspective, conclusions drawn from parasite‐

free laboratory populations might not reﬂect the response of

natural ﬁeld populations that are affected by parasites. This is

particularly relevant for parameters that are used to determine

safety limits of substances like LC50 and lowest or no observed

effect concentrations. These values might be considerably dif-

ferent if determined with parasite‐free test organisms or if para-

site infection is included, therefore including parasites in

ecotoxicological studies will provide a more realistic assessment

of stressor effects in a natural environment. Such experiments, in

which parasite infection is controlled, are less problematic if an

infection can be detected easily, such as for acanthocephalan

cystacanth larvae in amphipods that can be observed in the living

host, and host individuals can be selected according to the ex-

perimental design (Grabner & Sures, 2019). Nevertheless, most

parasites are visible only after the dissection of the host and the

use of further diagnostic techniques such as molecular detection.

In the latter case, initial parasitological screening of ﬁeld pop-

ulations will help to estimate the prevalence of parasites in the

population and help in planning experiments. Test organisms

should then be analysed for parasites at the end of the experi-

ment to be able to elucidate potential parasite effects on the

selected endpoints. Alternatively, experimental infections of

laboratory‐cultured test organisms can be conducted in the

course of ecotoxicological experiments if appropriate protocols

for a standardized infection are developed.

In addition to protist or metazoan parasites, there are sev-

eral pathogens such as viruses and bacteria that rarely have

been considered as an inﬂuencing factor in ecotoxicological

studies because their impact on the host is often not known (for

amphipods, see Bojko & Ovcharenko, 2019; for Daphnia, see

Stirnadel & Ebert, 1997). Those pathogens and further, un-

described parasites have to be characterized in more detail to

know the full “inventory”of the test organisms.

CONCLUSION

If we want to understand ecosystem processes, including

the effects of toxic substances on organisms and populations,

we need to consider parasites as integral parts of ecosystems

to get a reliable estimation of pollutant effects under real‐life

conditions and to determine the safety limits of chemicals that

reﬂect the responses of natural populations. We therefore

should consider naturally occurring parasites when using test

organisms from the ﬁeld and, if possible, also conduct tests

with laboratory‐infected hosts in addition to other stressors.

Acknowledgments—The present study was performed within

the Collaborative Research Center (CRC) 1439 RESIST (sub-

project A09) funded by the Deutsche Forschungsgemeinschaft

(DFG, German Research Foundation)—CRC 1439/1—project

number: 426547801. Open Access funding enabled and

organized by the open access publication fund of the University

of Duisburg‐Essen (Projekt DEAL).

Conﬂict of Interest—The authors declare no conﬂict of interest.

10 Environmental Toxicology and Chemistry, 2023;00:1–14—Grabner et al.

Author Contribution Statement—Daniel Grabner: Conceptu-

alization; Writing—original draft; Writing—review & editing.

Louisa E. Rothe: Visualization; Writing—original draft;

Writing—review & editing. Bernd Sures: Conceptualization;

Funding acquisition; Writing—original draft; Writing—review &

editing.

Data Availability Statement—No original data was produced

for this review article.

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Acanthocephalans as pollutant sinks? Higher pollutant accumulation in parasites may relieve their crustacean host

Article

Full-text available

Dec 2024

Increasing chemical pollution calls for a closer look at ecologically highly relevant host-parasite interactions to understand the persistence of organisms and populations in a polluted environment. The impact of chemical exposure within the host-parasite interactions – particularly the distinctive bioaccumulation behavior of organic micropollutants – can substantially influence the persistence of a species. This significance has been emphasized by previous research showing a higher tolerance of Gammarus roeselii (Amphipoda, Crustacea) infected with acanthocephalans during acute exposure to a pyrethroid. This suggests the presence of infection-related benefits within polluted environments. The present study addressed this complex relationship by investigating the chemical body burden and internal pollutant concentrations of both G. roeselii and its acanthocephalan parasites across a pollution gradient. Specifically, we analyzed 405 organic micropollutants and identified 123 of these in gammarids and their acanthocephalan parasites. Among the detected compounds, 22 are either banned or are no longer permitted for use in Germany. Remarkably, we discovered that the concentrations of pollutants were up to 35 times higher in the acanthocephalan parasites than in their crustacean intermediate hosts. The log KOW, the most frequently used measure of chemical hydrophobicity, could not explain the accumulation. Instead, the accumulation is likely explained by the unique physiology and high absorption capacity of acanthocephalans, combined with potentially limited biotransformation and excretion ability. This results in a redistribution of micropollutants within the host-parasite system, reducing the burden on the host up to 13.9% and potentially explaining the observed helpful effects of parasitized G. roeselii in polluted environments. Our study underscores the often overlooked but significant role of host-parasite interactions in human-altered ecosystems, revealing how these relationships can mediate and amplify the impacts of micropollutants within aquatic communities. These insights stress the need to consider the pervasive influence of metazoan parasites in environmental assessments and pollution management strategies.

Food Safety: Pathological and Biochemical Responses of Nile Tilapia (Oreochromis niloticus) to Parasitological Infestation and Heavy Metals Pollution in Aquaculture System, Jeddah, Saudi Arabia

Article

Full-text available

Dec 2024

Objective: The study aims to assess the overall safety of cultured tilapias in Jeddah City, Saudi Arabia by assessing the impact of infection and anthropogenic pollution on farmed tilapias based on fish sex, body weight, length, and heavy metals contamination. Materials and methods: A total of 111 fish were collected from an aquaculture farm in Hada Al-Sham, Jeddah, Saudi Arabia. Physicochemical parameters of water from the culture system were evaluated. Both ecto- and endoparasites were checked. Haematological, biochemical and histopathological investigations were evaluated. In addition, heavy metals, namely, cadmium (Cd), chromium (Cr), copper (Cu), nickel (Ni), lead (Pb), and zinc (Zn) were evaluated in different fish tissues and water samples from the aquaculture system. Results: The study revealed stressed aquaculture system. Tilapias were infested by both ectoparasites including Trichodina, Icthyophthirius multifiliis, Dactylogrus, and Cichlidogyrus, and endoparasites as Icthyophonus hoferi, the nematode Capillaria and coccidian protozoa. The study showed that male tilapias had greater infestation rates than females and longer and heavier male fish tended to be more susceptible to Dactylogyrus infection. Infected fish showed altered biochemical markers with subsequent increases in inflammatory and oxidative stress markers. The post-mortem lesion in the skin, gill lamellae, intestine, spleen, and liver showed significant pathological remarks. All investigated fish tissues revealed higher rates of heavy metals bioaccumulation compared to the surrounding waters. On the other hand, infected Nile tilapia tissues showed higher rate of metals accumulation compared to non-infected ones. Metals accumulated at a higher rate in the liver followed by kidney, intestine, gills, and muscles, respectively. Conclusions: This study is recognized as the first to address the food safety of farmed tilapias in Jeddah, Saudi Arabia. The results emphasized a significant relation between parasites and heavy metal in disrupting fish defense systems and harming fish’s physiological homeostasis and the histological state of tissues. The parasitized and polluted farmed fish pose health risk to humans due to possible zoonosis from parasitic infections and its subsequent bacterial infections with long-term exposure to toxic chemicals. Addressing the need for a combination of improved aquaculture practices, and stringent regulatory oversight.

Impact of multiple-factors on health and infections in marine mussels (Perumytilus purpuratus) inhabiting contaminated sites in the Humboldt Current System

Article

Full-text available

Feb 2025

Marine organisms are increasingly exposed to a combination of environmental stressors. However, most studies focus on single factors, limiting our understanding of real-world ecological challenges. This study investigates the combined effects of metal pollution, parasites, pathogens, and environmental variables on the health of Perumytilus purpuratus, a mussel species inhabiting the coast of northern Chile. The upwelling system in this area, combined with low water turnover, creates a unique environment in which to study how multiple factors interact. Mussels were sampled from several sites affected by metal discharges. Analyses revealed that individuals from central and northern sites exhibited the highest levels of parasites, pathogens, and tissue lesions. These health impacts were strongly associated with elevated pH, salinity, cadmium and copper concentrations in the water. Findings emphasise the synergistic effects of chemical and abiotic factors, underscoring the importance of incorporating multiple factors interactions into monitoring programmes. Such an approach can enhance predictions of ecological responses, inform conservation efforts, and guide policies addressing global challenges like aquatic pollution. Our study provides critical insights into how combined factors threaten aquatic ecosystems, offering a framework for more comprehensive environmental assessment.

Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics

Article

Full-text available

Feb 2025

Chemical exposure in the environment can adversely affect the biodiversity of living organisms, particularly when persistent chemicals accumulate over time and disrupt the balance of microbial populations. In this study, we examined how chemical contaminants influence microorganisms in sediment and overlaying water samples collected from the Kinnickinnic, Milwaukee, and Menomonee Rivers near Milwaukee, Wisconsin, USA. We characterized these samples using shotgun metagenomic sequencing to assess microbiome diversity and employed chemical analyses to quantify more than 200 compounds spanning 16 broad classes, including pesticides, industrial products, personal care products, and pharmaceuticals. Integrative and differential comparative analyses of the combined datasets revealed that microbial density, approximated by adjusted total sequence reads, declined with increasing total chemical concentrations. Protozoan, metazoan, and fungal populations were negatively correlated with higher chemical concentrations, whereas certain bacterial (particularly Proteobacteria) and archaeal populations showed positive correlations. As expected, sediment samples exhibited higher concentrations and a wider dynamic range of chemicals compared to water samples. Varying levels of chemical contamination appeared to shape the distribution of microbial taxa, with some bacterial, metazoan, and protozoan populations present only at certain sites or in specific sample types (sediment versus water). These findings suggest that microbial diversity may be linked to both the type and concentration of chemicals present. Additionally, this study demonstrates the potential roles of multiple microbial kingdoms in degrading environmental pollutants, emphasizing the metabolic versatility of bacteria and archaea in processing complex contaminants such as polyaromatic hydrocarbons and bisphenols. Through functional and resistance gene profiling, we observed that multi-kingdom microbial consortia—including bacteria, fungi, and protozoa—can contribute to bioremediation strategies and help restore ecological balance in contaminated ecosystems. This approach may also serve as a valuable proxy for assessing the types and levels of chemical pollutants, as well as their effects on biodiversity.

Locomotor activity and physiological responses of parasite-infected Gammarus fossarum exposed to the herbicide metazachlor

Article

Nov 2024
ENVIRON POLLUT

Insight into the effect of the ectoparasites on estimating the ontogenetic accumulation of trace and rare earth elements in fish: A case study of Mackerel icefish (Champsocephalus gunnari)

Article

Nov 2024
ENVIRON RES

The ontogenetic bioaccumulation of trace elements in marine species is influenced by both biotic and abiotic factors , including parasitic infestation. The Mackerel icefish (Champsocephalus gunnari) plays a significant role in the Antarctic ecosystem. Yet the impact of parasites on trace element accumulation in this species remains unclear. This study aims to gain insight into the ontogenetic accumulation patterns of trace elements in C. gunnari and how parasitic infestations affect these patterns. Two ectoparasites (Eubrachiella antarctica and Notobdella notothe-niae) were found on C. gunnari, but no endoparasites were detected. Concentrations of 34 elements in C. gunnari were analyzed, including essential elements (e.g. Yb). Major essential elements, such as magnesium (Mg, 1420-2380 μg g −1) and calcium (Ca, 436-1850 μg g −1), were significantly higher than minor elements like zinc (Zn, 19.5-29.3 μg g −1) and iron (Fe, 6.59-19.4 μg g −1) in both infested and non-infested fish. Strontium (Sr), though a non-essential element exhibited concentrations comparable to Fe of ranging from 2.45 to 13.6 μg g −1. Although the rare earth elements were detected, their concentrations were significantly lower, several orders of magnitude below those of the major and trace elements. Scandium (Sc, 0.06-0.27 μg g −1) was the only rare earth element comparable in magnitude to certain trace elements. Parasitic infestation altered the relationships between certain elements (e.g., P, Zn, and Dy) and fish length, as well as (e.g., Li, Co, Cu, and Sr) with fish weight. Nevertheless, all elements displayed consistent relationships with the condition factor, regardless of parasitic infestation, indicating that it remains a reliable indicator of trace element bioaccumulation in C. gunnari, even in the presence of ectoparasites.

Genetic Variability of Two Evolutionary Distinct Classes of the Acanthocephala Isolated from European Chub from Rivers of the Adriatic and Black Sea Basins in Croatia

Article

Full-text available

Sep 2024

The aim of our study was to investigate the genetic variability of two members of two evolutionary different classes of the Acanthocephala, Eoacanthocephala ( Neoechinirhynchus sp.) and Palaeacanthocephala ( Acanthocephalus sp.) from the same host, Squalius cephalus , from rivers of the Adriatic (rivers in Lika region: Lika, Novčica, Bogdanica and Jadova) and the Black Sea basins (Medsave location on the Sava River) in Croatia. The samples were collected from May 2021 to July 2022. To put the genetic position of the analyzed acanthocephalans in a broader context, the COI sequences of other specimens from the NCBI GenBank were used. BLAST analysis of partial COI sequences of acanthocephalans showed the presence of two different species: Acanthocephalus sp. and Neoechinorhynchus sp. Acanthocephalus sp. specimens did not show different grouping related to geographical origin (Bogdanica, Lika, Jadova) or Black Sea basin (Medsave-Sava River). Acanthocephalus cluster was subdivided into five main subclusters and 13 haplotypes were determined. When we compared our haplotypes with those from the NCBI GenBank, our haplotypes were closer to the A. anguillae specimens from the Kupa River and Dobra River in Croatia, and also to the haplotypes from Austria. For the species Neoechinorhynchus sp. from the Lika River and the specimens from the NCBI GenBank, four haplotypes were found out of five specimens. This genus was recorded for the first time in the Lika River area and for the first time in European chub in Croatia. The closest species Neoechinorhynchus sp. from Austria and Finland were grouped separately. Due to the lack of NCBI GenBank data for this species from other geographical regions, our data could not be compared. This shows that the taxonomy of the genus Neoechinorhynchus from Europe remains a challenge and underlines the need for further DNA sequence data and in-depth morphological study.

One like all? Behavioral response range of native and invasive amphipods to neonicotinoid exposure

Article

May 2024

Native and invasive species often occupy similar ecological niches and environments where they face comparable risks from chemical exposure. Sometimes, invasive species are phylogenetically related to native species, e.g. they may come from the same family and have potentially similar sensitivities to environmental stressors due to phylogenetic conservatism and ecological similarity. However, empirical studies that aim to understand the nuanced impacts of chemicals on the full range of closely related species are rare, yet they would help to comprehend patterns of current biodiversity loss and species turnover. Behavioral sublethal endpoints are of increasing ecotoxicological interest. Therefore, we investigated behavioral responses (i.e., change in movement behavior) of the four dominant amphipod species in the Rhine-Main area (central Germany) when exposed to the neonicotinoid thiacloprid. Moreover, beyond species-specific behavioral responses, ecological interactions (e.g. parasitation with Acanthocephala) play a crucial role in shaping behavior, and we have considered these infections in our analysis. Our findings revealed distinct baseline behaviors and species-specific responses to thiacloprid exposure. Notably, Gammarus fossarum exhibited biphasic behavioral changes with hyperactivity at low concentrations that decreased at higher concentrations. Whereas Gammarus pulex, Gammarus roeselii and the invasive species Dikerogammarus villosus, showed no or weaker behavioral responses. This may partly explain why G. fossarum disappears in chemically polluted regions while the other species persist there to a certain degree. But it also shows that potential pre-exposure in the habitat may influence behavioral responses of the other amphipod species, because habituation occurs, and potential hyperactivity would be harmful to individuals in the habitat. The observed responses were further influenced by acanthocephalan parasites, which altered baseline behavior in G. roeselii and enhanced the behavioral response to thiacloprid exposure. Our results underscore the intricate and diverse nature of responses among closely related amphipod species, highlighting their unique vulnerabilities in anthropogenically impacted freshwater ecosystems.

Influence of salinity on the thermal tolerance of aquatic organisms

Article

Full-text available

Sep 2024
SCI TOTAL ENVIRON

Aquatic organisms are challenged by changes in their external environment, such as temperature and salinity fluctuations. If these variables interacted with each other, the response of organisms to temperature changes would be modified by salinity and vice versa. We tested for potential interaction between temperature and salinity effects on freshwater, brackish, and marine organisms, including algae, macrophytes, heterotrophic protists, parasites, invertebrates, and fish. We performed a meta-analysis that compared the thermal tolerance (characterised by the temperature optimum, lower and upper temperature limits, and thermal breadth) at various salinities. The meta-analysis was based on 90 articles (algae: 15; heterotrophic protists: 1; invertebrates: 43; and fish: 31). Studies on macrophytes and parasites were lacking. We found that decreasing salinity significantly increased and decreased the lower and upper temperature limits, respectively, in all groups. Thus, a lowered salinity increased the thermal sensitivity of organisms. These findings mainly reflect the response of brackish and marine organisms to salinity changes, which dominated our database. The few studies on freshwater species showed that their lower thermal limits increased and the upper thermal limits decreased with increasing salinity, albeit statistically nonsignificant. Although non-significant, the response of thermal tolerance to salinity changes differed between various organism groups. It generally decreased in the order of: algae > invertebrates > fish. Overall, our findings indicate adverse effects of salinity changes on the temperature tolerance of aquatic organisms. For freshwater species, studies are comparatively scarce and further studies on their thermal performance at various salinity gradients are required to obtain more robust evidence for interactions between salinity and temperature tolerance. Considering test conditions such as acclimation temperature and potential infection with parasites in future studies may decrease the variability in the relationship between salinity and thermal tolerance.

Leeches Baicalobdella torquata feed on hemolymph but have a low effect on the cellular immune response of amphipod Eulimnogammarus verrucosus from Lake Baikal

Article

Full-text available

May 2024

Lake Baikal is one of the largest and oldest freshwater reservoirs on the planet with a huge endemic diversity of amphipods (Amphipoda, Crustacea). These crustaceans have various symbiotic relationships, including the rarely described phenomenon of leech parasitism on amphipods. It is known that leeches feeding on hemolymph of crustacean hosts can influence their physiology, especially under stressful conditions. Here we show that leeches Baicalobdella torquata (Grube, 1871) found on gills of Eulimnogammarus verrucosus (Gerstfeldt, 1858), one of the most abundant amphipods in the Baikal littoral zone, indeed feed on the hemolymph of their host. However, the leech infection had no effect on immune parameters such as hemocyte concentration or phenoloxidase activity and also did not affect glycogen content. The intensity of hemocyte reaction to foreign bodies in a primary culture was identical between leech-free and leech-infected animals. Artificial infection with leeches also had only a subtle effect on the course of a model microbial infection in terms of hemocyte concentration and composition. Despite we cannot fully exclude deleterious effects of the parasites, our study indicates a low influence of a few leeches on E. verrucosus and shows that leech-infected amphipods can be used at least for some types of ecophysiological experiments.

Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala

Article

Full-text available

Jun 2023
Parasite

Although interest in Acanthocephala seems to have reached only a small community of researchers worldwide, we show in this opinion article that this group of parasites is composed of excellent model organisms for studying key questions in parasite molecular biology and cytogenetics, evolutionary ecology, and ecotoxicology. Their shared ancestry with free-living rotifers makes them an ideal group to explore the origins of the parasitic lifestyle and evolutionary drivers of host shifts and environmental transitions. They also provide useful features in the quest to decipher the proximate mechanisms of parasite-induced phenotypic alterations and better understand the evolution of behavioral manipulation. From an applied perspective, acanthocephalans’ ability to accumulate contaminants offers useful opportunities to monitor the impacts – and evaluate the possible mitigation – of anthropogenic pollutants on aquatic fauna and develop the environmental parasitology framework. However, exploring these exciting research avenues will require connecting fragmentary knowledge by enlarging the taxonomic coverage of molecular and phenotypic data. In this opinion paper, we highlight the needs and opportunities of research on Acanthocephala in three main directions: (i) integrative taxonomy (including non-molecular tools) and phylogeny-based comparative analysis; (ii) ecology and evolution of life cycles, transmission strategies and host ranges; and (iii) environmental issues related to global changes, including ecotoxicology. In each section, the most promising ideas and developments are presented based on selected case studies, with the goal that the present and future generations of parasitologists further explore and increase knowledge of Acanthocephala.

The Asymmetric Response Concept explains ecological consequences of multiple stressor exposure and release

Article

Full-text available

Feb 2023
SCI TOTAL ENVIRON

Our capacity to predict trajectories of ecosystem degradation and recovery is limited, especially when impairments are caused by multiple stressors. Recovery may be fast or slow and either complete or partial, sometimes result in novel ecosystem states or even fail completely. Here, we introduce the Asymmetric Response Concept (ARC) that provides a basis for exploring and predicting the pace and magnitude of ecological responses to, and release from, multiple stressors. The ARC holds that three key mechanisms govern population, community and ecosystem trajectories. Stress tolerance is the main mechanism determining responses to increasing stressor intensity, whereas dispersal and biotic interactions predominantly govern responses to the release from stressors. The shifting importance of these mechanisms creates asymmetries between the ecological trajectories that follow increasing and decreasing stressor intensities. This recognition helps to understand multiple stressor impacts and to predict which measures will restore communities that are resistant to restoration.

Effects of multiple stressors in fish: How parasites and contaminants interact

Article

Full-text available

Aug 2022

Interest in local environmental conditions and the occurrence and behaviour of parasites has increased over the last 3 decades, leading to the discipline of Environmental Parasitology. The aim of this discipline is to investigate how anthropogenically altered environmental factors influence the occurrence of parasites and how the combined effects of pollutants and parasites affect the health of their hosts. Accordingly, in this paper, we provide an overview of the direct and indirect effects of pollutants on the occurrence and distribution of fish parasites. However, based on current knowledge, it is difficult to draw general conclusions about these interdependencies, as the effects of pollutants on free-living (larval) parasite stages, as well as their effects on ectoparasites, depend on the pollutant–host–parasite combination as well as on other environmental factors that can modulate the harmful effects of pollutants. Furthermore, the question of the combined effects of the simultaneous occurrence of parasites and pollutants on the physiology and health of the fish hosts is of interest. For this purpose, we differentiate between the dominance effects of individual stressors over other, additive or synergistically reinforcing effects as well as combined antagonistic effects. For the latter, there are only very few studies, most of which were also carried out on invertebrates, so that this field of research presents itself as very promising for future investigations.

Dysbiosis of fish gut microbiota is associated with helminths parasitism rather than exposure to PAHs at environmentally relevant concentrations

Article

Full-text available

Jun 2022

Although parasite infection and pollution are common threats facing wild populations, the response of the gut microbiota to the joint impact of these stressors remains largely understudied. Here, we experimentally investigated the effects of exposure to Polycyclic Aromatic Hydrocarbons (PAHs) and infection by a common acanthocephalan intestinal parasite (Pomphorhynchus sp.) on the gut microbial flora of a freshwater fish, the European chub (Squalius cephalus). Naturally infected or uninfected individuals were exposed to PAHs at environmentally realistic concentrations over a five-week period. Characterization of the gut bacterial community through 16S rRNA gene amplicon sequencing revealed that parasitic infection was a more structuring factor of bacterial diversity and composition than PAH exposure. Specifically, chub infected by Pomphorhynchus sp. harbored significantly less evenly represented gut bacterial communities than the uninfected ones. In addition, substantial changes in sequence abundance were observed within the main bacterial phyla, including the Firmicutes, Fusobacteriota, Actinobacteriota, and Proteobacteria. Again, these compositional changes correlated with host infection with Pomphorhynchus sp., confirming its pivotal role in gut microbial assemblage. Overall, these results highlight the importance of defining the parasitic status of individuals when conducting microbial ecotoxicological analyses at the digestive tract level, as this should lead to better understanding of microbiota modulations and help to identify microbial markers specifically associated with chemicals.

Effects of Schyzocotyle acheilognathi (Yamaguti, 1934) infection on the intestinal microbiota, growth and immune reactions of grass carp (Ctenopharyngodon idella)

Article

Full-text available

Apr 2022
PLOS ONE

Our understanding of interactions among intestinal helminths, gut microbiota and host is still in its infancy in fish. In this study, the effects of Schyzocotyle acheilognathi infection on the intestinal microbiota, growth and immune reactions of grass carp were explored under laboratory conditions. 16S rDNA amplification sequencing results showed that S. acheilognathi infection altered the composition of intestinal microbiota only at the genus level, with a significant increase in the relative abundance of Turicibacter and Ruminococcus (P < 0.05) and a significant decrease in the relative abundance of Gordonia, Mycobacterium and Pseudocanthomonas (P < 0.05). Schyzocotyle acheilognathi infection had no significant effect (P > 0.05) on the alpha diversity indices (including Chao1, ACE, Shannon, Simpson index) of intestinal microbiota in grass carp, but PERMANOVA analysis showed that microbial structure significantly (P < 0.01) differed between hindgut and foregut. PICRUST prediction showed that some metabolism-related pathways were significantly changed after S. acheilognathi infection. The relative abundance of Turicibacter was positively correlated with the fresh weight of tapeworm (foregut: r = 0.48, P = 0.044; hindgut: r = 0.63, P = 0.005). There was no significant difference in the body condition of grass carp between the S. acheilognathi infected group and the uninfected group (P > 0.05). Intestinal tissue section with HE staining showed that S. acheilognathi infection severely damaged the intestinal villi, causing serious degeneration, necrosis and shedding of intestinal epithelial cells. The real-time fluorescent quantitative PCR results showed that S. acheilognathi infection upregulated the mRNA expression of the immune-related genes: Gal1−L2, TGF−β1 and IgM.

Parasite infection influences the biomarker response and locomotor activity of Gammarus fossarum exposed to conventionally-treated wastewater

Article

Full-text available

May 2022
ECOTOX ENVIRON SAFE

Modern wastewater treatment plants cannot completely remove pollutants. Often, effluents entering the aquatic environment still contain micropollutants such as pharmaceuticals or pesticides, which may impose adverse effects on aquatic biota. At the same time, a large proportion of free-living aquatic species are known to be infected with parasites, which raises the question of interactions between environmental stressors (such as micropollutants) and parasite infection. We chose the freshwater amphipod Gammarus fossarum (Koch, 1835) as a test organism to investigate potential pollutant-parasite interactions. This gammarid is frequently used in ecotoxicological tests and is also commonly infected with larvae of the acanthocephalan parasite species Polymorphus minutus (Zeder, 1800) Lühe, 1911. We exposed infected and uninfected specimens of G. fossarum to conventionally-treated wastewater and river water in a 22-day flow channel experiment. The test organisms’ response was measured as mortality rates, concentrations or activities of five biomarkers, and overall locomotor activity. No significant differences were found between mortality rates of different exposure conditions. Contrastingly, three biomarkers (phenoloxidase activity, glycogen, and lipid concentrations) showed a significant increase in infected gammarids, while the effect of the water type was insignificant. Infected gammarids also showed a significantly higher locomotor activity in both water types. Our results suggest that the response of G. fossarum during the exposure experiments was mainly driven by parasite infection. This implies that parasites may act as additional biotic stressors in multiple stressor scenarios, and therefore, might play an important role when measuring the response of organisms to chemical stressors. Future ecotoxicological studies and assessments thus should consider parasite infection as an additional test parameter.

Environmental parasitology: stressor effects on aquatic parasites

Article

Apr 2023

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host-parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host-parasite systems.

Pollutant load and ecotoxicological effects of sediment from stormwater retention basins to receiving surface water on Lumbriculus variegatus

Article

Nov 2022
SCI TOTAL ENVIRON

The overflow of stormwater retention basins during intense and prolonged precipitation events may result in the direct input of particulate pollutants and remobilization of already sedimented particle-bound pollutants to receiving freshwater bodies. Particle-bound pollutants may cause adverse effects on aquatic biota, particularly sediment dwellers. Therefore, we investigated the sediment pollution load of a stream connected to the outfalls of two stormwater basins to determine the impact of the basins' discharges on the metal and organic pollutant content of the sediment. Also, the possible adverse effects of the pollutant load on benthic dwellers were evaluated in sediment toxicity tests with Lumbriculus variegatus and the effects on its growth, reproduction and the biomarkers catalase, acetylcholinesterase and metallothionein were analyzed. The results showed that the retention basins contained the highest load of pollutants. The pollutant load in the stream did not show a clear pollution pattern from the inlets. However, metal enrichment ratios revealed contamination with Cu, Pb and Zn with Pb and Zn above threshold effect concentrations in all sites. Ecotoxicity results showed that the retention basin samples were the most toxic compared to sediment from the stream. Exposure experiments with the stream sediment did not show considerable effects on reproduction, catalase activity and metallothionein concentration. However, modest inhibitions of growth and activity of acetylcholinesterase were detected. Based on the observed results, it cannot be concluded that overflows of the retention basin are responsible for the pollutant contents downstream of their inlet. Other sources that were not considered in this study, such as diffuse input, historic pollution and point sources further upstream as well as along the stream, are likely the major contributors of pollutant load in the sediment of the studied transects of the stream. Additionally, the observed results in the stormwater basin sediment further highlight their importance in retaining particle-bound pollutants and preventing ecotoxicological effects from receiving surface water bodies.

The trematode Podocotyle atomon modulates biochemical responses of Gammarus locusta to thermal stress but not its feeding rate or survival

Article

Nov 2022
SCI TOTAL ENVIRON

Although parasitism is one of the most common species interactions in nature, the role of parasites in their hosts' thermal tolerance is often neglected. This study examined the ability of the trematode Podocotyle atomon to modulate the feeding and stress response of Gammarus locusta towards temperature. To accomplish this, infected and uninfected females and males of Gammarus locusta were exposed to temperatures (2, 6, 10, 14, 18, 22, 26, 30 °C) for six days. Shredding (change in food biomass) and defecation rates (as complementary measure to shredding rate) were measured as proxies for feeding activity. Lipid and glycogen concentrations (energy reserves), catalase (oxidative stress indicator), and phenoloxidase (an immunological response in invertebrates) were additionally measured. Gammarid survival was optimal at 10 °C as estimated by the linear model and was unaffected by trematode infection. Both temperature and sex influenced the direction of infection effect on phenoloxidase. Infected females presented lower phenoloxidase activity than uninfected females at 14 and 18 °C, while males remained unaffected by infection. Catalase activity increased at warmer temperatures for infected males and uninfected females. Higher activity of this enzyme at colder temperatures occurred only for infected females. Infection decreased lipid content in gammarids by 14 %. Infected males had significantly less glycogen than uninfected, while infected females showed the opposite trend. The largest infection effects were observed for catalase and phenoloxidase activity. An exacerbation of catalase activity in infected males at warmer temperatures might indicate (in the long-term) unsustainable, overwhelming, and perhaps lethal conditions in a warming sea. A decrease in phenoloxidase activity in infected females at warmer temperatures might indicate a reduction in the potential for fighting opportunistic infections. Results highlight the relevance of parasites and host sex in organismal homeostasis and provide useful insights into the organismal stability of a widespread amphipod in a warming sea.

Microsporidia: a new taxonomic, evolutionary, and ecological synthesis

Article

Jun 2022
Trends Parasitol

Microsporidian diversity is vast. There is a renewed drive to understand how microsporidian pathological, genomic, and ecological traits relate to their phylogeny. We comprehensively sample and phylogenetically analyse 125 microsporidian genera for which sequence data are available. Comparing these results with existing phylogenomic analyses, we suggest an updated taxonomic framework to replace the inconsistent clade numbering system, using informal taxonomic names: Glugeida (previously clades 5/3), Nosematida (4a), Enterocytozoonida (4b), Amblyosporida (3/5), Neopereziida (1), and Ovavesiculida (2). Cellular, parasitological, and ecological traits for 281 well-defined species are compared with identify clade-specific patterns across long-branch Microsporidia. We suggest that future taxonomic circumscriptions of Microsporidia should involve additional markers (SSU/ITS/LSU), and that a comprehensive suite of phenotypic and ecological traits help to predict broad microsporidian functional and lineage diversity.

Parasites and Pollutants: Effects of Multiple Stressors on Aquatic Organisms

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