Supplementary material Combined effects of parasites and contaminants on animal health: parasites do matter




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Supplementary material
Combined effects of parasites and contaminants on animal health: parasites do matter

David J. Marcogliese1 and Michael Pietrock2

1 Fluvial Ecosystem Research Section, Aquatic Ecosystem Protection Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment Canada, St. Lawrence Centre, 105 McGill, 7th Floor, Montreal, Quebec,

Canada H2Y 2E7



2 Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N 5B3

Corresponding author: Marcogliese, D.J. (david.marcogliese@ec.gc.ca)
Table S1. Lethal effects of combined exposure to parasites and other stressors. Selected examples of enhanced mortality due to combined exposure to natural or anthropogenic stressors in conjunction with parasitism.


Host species

Stressor

Parasite

Parasite taxon

Refs.




Natural stressors










Periwinkle (Littorina littorea)

Increased temperature

Cryptocotyle lingua

Trematoda

[S1]

Mud-flat snail [Ilyanassa (=Nassarius) obsoleta]

Increased temperature

Lepocreadium ovalis, Zoogonus rubellus

Trematoda

[S2]

Snail (Nassarius reticulatus)

Decreased or Increased temperature

Various

Trematoda

[S3]

Snail (Biomphalaria glabrata)

Increased temperature

Schistosoma mansoni

Trematoda

[S4]

Mud snail (Hydrobia neglecta)

Dessication

Microphallidae

Trematoda

[S5]

Salt marsh snail (Cerithidea californica)

Decreased oxygen

Various

Trematoda

[S6]




Increased temperature

Various

Trematoda

[S6]

Cockle (Cerastoderma edule)

Decreased oxygen

Himasthla elongata

Trematoda

[S7]

Water flea (Daphnia galeata)

Predator cues

Caullerya mesnili

Microparasite

[S8]

Water flea (Daphnia magna)

Starvation

Glugoides intestinalis

Microsporidia

[S9]




Increased temperature

Pasteuria ramosa

Bacteria

[S10]

Kelp shrimp (Eualus suckleyi)

Salinity change

Bopyroides hippolytes

Isopoda

[S11]

Oyster (Crassostrea gigas)

Mechanical stress, stress hormones

Vibrio splendidus

Bacteria

[S12]

European eel (Anguilla anguilla)

Decreased oxygen

Anguillicoloides (= Anguillicola) crassus

Nematoda

[S13,S14]

Three-spined stickleback (Gasterosteus aculeatus)

Reduced diet

Schistocephalus solidus

Cestoda

[S15,S16]

Chinook salmon (Oncorhynchus tshawytscha)

Listonella anguillarum (bacteria)

Nanophyetus salmincola

Trematoda

[S17]

Sockeye salmon (Oncorhynchus nerka)

Increased salinity

Eubothrium salvelini

Cestoda

[S18]

Bridled goby (Coryphopterus glaucofraenum)

High density, refuge shortage

Pharodes tortugensis

Copepoda

[S19]

Ruffe (Gymnocephalus cernuus)

Decreased oxygen

Spinitectus gracilus, Acanthostomum sp., Strigeidae, and various other helminths

Nematoda, Trematoda

[S20]

Mosquitofish (Gambusia affinis)

Increased temperature

Bothriocephalus acheilognathi

Cestoda

[S21]

Bluegill (Lepomis macrochirus)

Decreased temperature

Uvulifer ambloplitis

Digenea

[S22]

Wood frog [Lithobates (=Rana) sylvaticus] tadpoles

Reduced diet; high density

Desserobdella picta

Hirudinea

[S23]

Leopard frog [Lithobates (=Rana) pipiens]

Increased temperature

Pseudomonas aeruginosa

Bacteria

[S24]

Red-legged frog (Rana aurora)

Predation

Candida micola

Yeast

[S25]




Lack of nitrates

Saprolegnia sp.

Fungus

[S26]

Western toad [Anaxyurus (=Bufo) boreas]; Cascades frog (Rana cascadae) - eggs

UV-B radiation

Saprolegnia sp.

Fungus

[S27]

Gray tree frog (Hyla versicolor)

Pond drying

Telorchis sp.

Trematoda

[S28]

Salamander (Ambystoma tigrinum) tadpoles

Decreased temperature

Ranavirus sp.

Virus

[S29]

Soay sheep (Ovis aries)

Reduced diet

Ostertagia spp.

Nematoda

[S30]

Snowshoe hare (Lepus americanus)

Predation


Obeliscoides cuniculi

Nematoda

[S31]




Anthropogenic stressors










Water flea (Daphnia magna)

Carbaryl, carbayl + predator

Pasteuria ramose, Flabelliforma magnivora

Bacteria

Microsporidia



[S32,S33]

Amphipod (Gammarus pulex)

Acidification

Pomphorhynchus laevis

Acanthocephala

[S34,S35]

Oyster (Crassostrea virginica)

Tributyltin (TBT)

Perkinsus marinus

Protozoa

[S36, S37]

Snail (Biomphalaria glabrata)

Cadmium, lead or mercury

Schistosoma mansoni

Trematoda

[S38]

Snail (Lymnaea stagnalis)

Zinc

Schistosomatidium douthitti; Trichobilharzia sp.

Trematoda

[S39]




Cadmium

Diplostomum spathaceum

Trematoda

[S40]

Snail (Lymnaea peregra)

Cadmium

Diplostomum spathaceum, Echinoparyphium recurvatum, Notocotylus attenuatus, or Sanguinicola inermis

Trematoda

[S40]

Sea fan (Gorgonia ventalina)

Eutrophication

Aspergillus sydowii

Fungus

[S41]

Coral (Montastraea spp.)

Eutrophication

Vibrio spp.

Bacteria

[S41]

Three-spined stickleback (Gasterosteus aculeatus)

Cadmium + reduced diet

Schistocephalus solidus

Cestoda

[S16]




Cadmium

Schistocephalus solidus

Cestoda

[S42]

Coho salmon (Oncorhynchus kisutch)

Crude oil, toluene or naphthalene

Anodonta oregonensis

Mollusca

[S43]




Sodium pentachlorophenate

Corynebacterium salmoninus

Bacteria

[S44]

Sockeye salmon (Oncorhynchus nerka)

Zinc

Eubothrium salvelini

Cestoda

[S45]

Tilapia (Oreochromis mossambicus)

Chromium

Aeromonas hydrophila

Bacteria

[S46]

Goldfish (Carassius auratus)

Pesticide mixture

Aeromonas hydrophila

Bacteria

[S47]

Atlantic cod (Gadus morhua)

Oil-contaminated water

Trypanosoma murmanensis

Protozoa

[S48]

Guppy (Poecilia reticulata)

Zinc

Gyrodactylus turnbulli

Monogenea

[S49]

Winter flounder (Pseudopleuronectes americanus)

Oil-contaminated sand

Trypanosoma murmanensis

Protozoa

[S48, S50]

Fish (Galaxias anomalus)

Glyphosate

Telogaster opisthorchis

Trematoda

[S51]

Red-legged frog (Rana aurora)

Nitrate

Saprolegnia sp.

Fungus

[S26]

Woodhouse’s toad [Anaxyurus (=Bufo) woodhousii]

Malathion

Aeromonas hydrophila

Bacteria

[S52]

Tiger salamander (Ambystoma tigrinum)

Atrazine, chlorpyrifos

A. tigrinum virus (ATV)

Virus

[S53]

Common loon (Gavia immer)

Mercury

Intestinal nematodes

Nematoda

[S54]


Table S2. Sublethal effects of combined exposure to parasites and other stressors. Selected examples of combined sublethal effects of natural or anthropogenic stressors and parasites on physiological function, life history characteristics and/or biomarkers of animal health.


Host species

Stressor

Parasite

Parasite taxon

Response/biomarker & effect a

Refs.




Natural stressors













Periwinkle (Littorina littorina)

Increased temperature

Renicola roscovita, Himasthla elongata, Cryptocotyle lingua

Trematoda

Increased rate of consumption in infected molluscs at higher temperature; reduced negative effect of parasites on grazing

[S55]

Snail (Biomphalaria glabrata)

Increased temperature

Schistosoma mansoni

Trematoda

Increased heart rate

[S4]

Snail (Nassarius reticulatus)

High temperature

Various

Trematoda

Increased oxygen consumption

[S3]

Manila clam (Ruditapes philippinarum)

Toxic algae (Prorocentrum minimum)

Perkinsus olseni

Protozoa

Pathology: atrophy and degeneration of ova, hyaline breakdown of muscle fibres

[S56]

Cockle (Cerastoderma edule)

Decreased oxygen

Himasthla elongata

Trematoda

Reduced burrowing ability

[S7]

Water flea (Daphnia galeata)

Predatory cues

Caullerya mesnili

Microparasite

Reduced age at maturity, fewer eggs at 2nd adult instar

[S8]

Water flea (Daphnia magna)

Increased temperature

Pasteuria ramosa

Bacteria

Increased rate of castration

[S57]

Sea urchin (Strongylocentrotus purpuratus)

Increased temperature

Black ring disease

Bacteria (?)

Increased pathology, reduced gonadal index

[S58]

Sockeye salmon (Oncorhynchus nerka)

Increased salinity

Eubothrium salvelini

Cestoda

Increased plasma sodium levels

[S18]

European eel (Anguilla anguilla)

Increased temperature

Anguillicoloides (= Anguillicola) crassus

Nematoda

Lag in glucose mobilisation, lack of haemoglobin response

[S59]

Wood frog [Lithobates (=Rana) sylvaticus] tadpoles

Increased temperature

Desserobdella picta

Hirudinea

Reduced growth rate

[S23]

Leopard frog [Lithobates (=Rana) pipiens]

Increased density

Echinostoma trivolvis

Trematoda

Reduced body size

[S60]

Red-legged frog (Rana aurora)

Predatory cues

Candida micola

Yeast

Reduced ability to differentiate cues

[S25]

Fowler’s toad [Anaxyurus (=Bufo) fowleri]; Gray tree frog (Hyla chrysoscelis)

Interspecific competition

Batrachochytrium dendrobatidis

Fungus

Reduced size at metamorphosis

[S61]

Gray tree frog (Hyla chrysoscelis)

Interspecific competition

Batrachochytrium dendrobatidis

Fungus

Slower development

[S61,S62]

Gray tree frog (Hyla versicolor)

Pond drying

Telorchis sp.

Trematoda

Reduced size at metamorphosis

[S28]

Long-toed salamander (Ambystoma macrodactylum)

Predation

Ribeiroia ondatrae

Trematoda

Increased frequency of limb malformations

[S63]

Common lizard (Lacerta vivipara)

Increased density

Haemogregarines

Protozoa

Increased plasma corticosterone

[S64]

Mallard (Anas platyrhynchos)

Crowding

Echinuria uncinata

Nematoda

Involution of bursa of Fabrcius & thymus gland, hypertrophy of adrenal gland, reduced growth

[S65]

Mouse (Mus musculus)

Temperature (cold), reduced diet

Heligmosomoides polygyrus

Nematoda

Reduced glucose uptake rate

[S66, S67]




Anthropogenic stressors













Zebra mussel (Dreissena polymorpha)

Industrial pollution

Assorted parasites

Assorted taxa

Smaller and more numerous lysosomes

[S68]

Pea clam (Pisidium amnicum)

Pentachlorphenol

Bunodera luciopercae

Trematoda

Reduced behavioural activity, lower metabolic rate

[S69, S70]

Cockle (Cerastoderma edule)

Cadmium

Labratrema minimus, Himasthla elongata

Trematoda

Increased metal contamination in tissue, lack of change or decreased metallothionein in tissue

[S71]

Water flea (Daphnia magna)

Carbaryl

Pasteuria ramosa

Bacteria

Accelerated castration, increased age at maturity, increased 1st brood fecundity, increased size at maturity

[S32, S33]




Carbaryl + predator

Pasteuria ramosa

Bacteria

Accelerated castration, increased age at maturity, increased 1st brood fecundity, increased size at maturity, increased body length, decreased population growth rate

[S32, S33]




Carbaryl

Flabelliforma magnivora

Microsporidia

Reduced fecundity

[S32]

Amphipod (Gammarus roeseli)

Palladium

Polymorphus minutus

Acanthocephala

Inhibition of heat shock protein hsp70

[S72]

Winter flounder (Pseudopleuronectes americanus)

Oil-contaminated sand

Trypanosoma murmanensis

Protozoa

Reduced condition factor, blood haemoglobin levels, blood packed cell volumes, gall bladder, spleen & testis somatic indices

[S48,S50]

Atlantic cod (Gadus morhua)

Oil-contaminated water

Trypanosoma murmanensis

Protozoa

Reduced liver somatic index, hematocrit

[S48]

Rainbow trout (Oncorhynchus mykiss)

Artificial confinement

Lepeophtheirus salmonis

Copepoda

Higher plasma & cortisol levels, reduced spleen somatic index, increased erythrocyte & lymphocyte numbers in blood, increased oxygen radical production

[S73]







Argulus foliaceus

Branchiura

Higher plasma ACTH & cortisol levels, decreased lysozyme activity, complement activity & oxygen radical production

[S74]

Chinook salmon (Oncorhynchus tshawytscha)

Aroclor 1254 (PCB)

Nanophyetus salmincola

Trematoda

Reduced anterior kidney plaque-forming cell response

[S17]

Arctic charr (Salvelinus alpinus)

Toxaphene

Diphyllobothrium dendriticum

Cestoda

Reduced growth, reduced condition, reduced muscle lipid and protein content

[S75]

European chub (Leuciscus cephalus)

Sewage effluent

Ligula intestinalis

Cestode

Reduced gonadosomatic index, lower gamete stage in males

[S76]

Carp (Cyprinus carpio)

Ammonia, cadmium

Sanguinicola inermis

Trematoda

Cellular disruption of thymus; reduced neutrophil, thrombocyte and leucocyte counts in pronephros; increased thrombocyte counts in thymus, increased eosinophil counts in thymus and pronephros

[S77, S78]




Copper

Ptychobothrium sp.

Cestoda

Reduced antibody in liver, increased antibody in plasma, increased lysozyme activity in head kidney & plasma

[S79]




Chitosan

Ptychobothrium sp.

Cestoda

Increased lysozyme activity in head kidney & plasma

[S79]




Copper + chitosan

Ptychobothrium sp.

Cestoda

Decreased ceruloplasmin activity in head kidney, decreased lysozyme activity in plasma, less reduction in activity of antioxidant enzymes

[S79,S80]

European eel (Anguilla anguilla)

Aquacultural stress (netting + handling)

Anguillicoloides (= Anguillicola) crassus

Nematoda

Increased glucose mobilisation and utilisation

[S81]




Cadmium + PCB

Anguillicoloides crassus

Nematoda

Increased cortisol levels in blood

[S82]

Striped bass (Morone saxatilis)

Zinc, benzene

Anisakis sp.

Nematoda

Reduced haematocrit

[S83]

California killifish (Fundulus parvipinnis)

Handling

Euhaplorchis californiensis

Trematoda

Increased serotonergic activity in raphe nuclei

[S84]

Yellow perch (Perca flavescens)

Industrial pollution

Raphidascaris acus

Apophallus brevis

Nematoda
Trematoda

Increased lipid peroxidation in liver
Increased lipid peroxidation in liver

[S85]









Diplostomum spp.




Decreased glutathione reductase activity in the gills

Increased catalase activity in the kidney



[S86]

Spottail shiner (Notropis hudsonius)

Industrial & urban pollution

Plagioporus sinitsini

Trematoda

Increased pigmented macrophages in spleen, reduced condition index

[S87]

Fathead minnow (Pimephales promelas)

Cadmium

Saprolegnia ferax

Fungus

Reduced number of epidermal club cells

[S88]

Fish (Galaxias anomalus)

Glyphosate

Telogaster opisthorchis

Trematoda

Increased spinal malformations

[S51]

Woodhouse’s toad [Anaxyurus (=Bufo) woodhousii]

Malathion

Aeromonas hydrophila

Bacteria

Cinical disease, hepatomegaly

[S52]

Gray treefrog (Hyla chrysoscelis) tadpoles

Copper

Batrachochytrium dendrobatidis

Fungus

Increased larval development time, decreased levels of brain cholinesterase

[S89]

Wood frog frog [Lithobates (=Rana) sylvaticus] tadpoles

Atrazine & Malathion

Ribeiroia sp., Telorchis sp.

Trematoda

Reduced body mass, increased limb deformities, reduced eosinophil numbers in blood

[S90]

Leopard frog [Lithobates (=Rana) pipiens]

Pesticide mixture

Rhabdias ranae

Nematoda

Reduced spleen cell concentration, reduced phagocytosis of spleen cells

[S91]

Bullfrog [Lithobates (=Rana) catesbeianus]

Agricultural pesticides

Haematoloechus sp.

Trematoda

Increased acetylcholinesterase in plasma, increased monocytes

[S92]

Loon (Gavia immer)

Mercury

Intestinal digeneans

Trematoda

Decreased body condition

[S54]

Rat (Rattus rattus)

Cadmium

Moniliformis moniliformis

Acanthocephala

Decreased cortisol levels in blood

[S93]

a Effect is measurement with combined parasite + stressor compared to effect of stressor alone.

Supplementary References
S1 McDaniel, S.J. (1969) Littorina littorea: Lowerd heat tolerance due to Cryptocotyle lingua. Exp. Parasitol. 25, 13-15

S2 Vernberg, W.B. and Vernberg, F.J. (1963) Influence of parasitism on thermal reistance of the mud-flat snail, Nassarius obselata Say. Exp. Parasitol. 14, 330-332

S3 Tallmark, B. and Norrgren, G. (1976) The influence of parasitic trematodes on the ecology of Nassarius reticulatus (L.) in Gullmar Fjord (Sweden). Zoon 4, 149-154.

S4 Lee, F.O. ansd Cheng, T.C. (1971) Schistosoma mansoni infection in Biomphalaria glabrata: Alterations in heart rate and thermal tolerance in the host. J. Invert. Pathol. 18, 412-418.

S5 Jensen, K.T. et al. (1996) The effect of larval trematodes on the survival rates of two species of mud snails (Hydrobiidae) experimentally exposed to dessication, freezing and anoxia. Helgoländer Meeresunters. 50, 327-335

S6 Sousa, W.P. and Gleason, M. (1989) Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia). Oecologia 80, 456-464

S7 Wegeberg, A.M. and Jensen, K.T. (1999) Reduced survivorship of Himasthla (Trematoda, Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. J. Sea Res. 42, 325-331

S8 Lass. S. and Bittner, K. (2002) Facing multiple enemies: Parasitised hosts respond to predator kairomones. Oecologia 132, 344-349

S9 Pulkkinen, K. and Ebert, D. (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85, 823-833

S10 Vale, P.F. et al. (2008) Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interacations. J. Evol. Biol. 21, 1418-1427

S11 Moles, A. and Pella, J.J. (1984) Effects of parasitism and temperature on salinity tolerance of the kelp shrimp Eualus suckleyi. Trans. Am. Fish. Soc. 113, 354-359

S12 Lacoste, A. et al. (2001) Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus. Appl. Environ. Microbiol. 67, 2304-2309

S13 Molnár, K. (1993) Effect of decreased oxygen content on eels (Anguilla anguilla) infected by Anguillicola crassus (Nematoda: Dracunculoidea). Acta Vet. Hung. 41, 349-360

S14 Lefebvre, F. et al. (2007) Interaction between the severity of the infection by the nematode Anguillicola crassus and the tolerance to hypoxia in the European eel Anguilla anguilla. Acta Parasitol. 52, 171-175

S15 Pascoe, D. and Mattey, D. (1977) Dietary stress in parasitzed and non-parasitized Gasterosteus aculeatus L. Z. Parasitenkd. 51, 179-186

S16 Pascoe, D. and Woodworth, J. (1980) The effects of joint stress on sticklebacks. Z. Parasitenkd. 62, 159-163

S17 Jacobson, K.C. et al. (2003) Cumulative effects of natural and anthropogenic stress on immune function and disease resistance in juvenile Chinook salmon. J. Aquat. Anim. Health 15, 1-12

S18 Boyce, N.P. and Clarke, W.C. (1983) Eubothrium salvelini (Cestoda: Pseudophyllidea) impairs seawater adaptation of migrant sockeye salmon yearlings (Oncorhynchus nerka) from Babine Lake, British Columbia. Can. J. Fish. Aquat. Sci. 40, 821-824

S19 Forrester, G.E. and Finley, R.J. (2006) Parasitism and a shortage of refuges jointly mediate the strength of density dependence in a reef fish. Ecology 87, 1110-1115

S20 Pronin, N.M. et al. (1997) Effect of parasites on resistance to oxygen starvation in the ruff (Gymnocephalus cernuus). Russ. J. Ecol. 28, 278-280

S21 Granath, W.O., Jr. and Esch, G.W. (1983) Survivorship and parasite-induced host mortality among mosquitofish in a predator-free, North Carolina cooling reservoir. Am. Midl. Nat. 110, 314-323

S22 Lemly, A.D. and Esch, G.W. (1984) Effects of the trematode Uvulifer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: Ecological implications. J. Parasitol. 70, 475-492

S23 Berven, K.A. and Boltz, R.S. (2001) Interactive effects of lech (Desserobdella picta) infection on wood frog (Rana sylvatica) tadpole fitness traits. Copeia 2001, 907-915

S24 Brodkin, M.A. et al. (1992) Response of Rana pipiens to graded doses of the bacterium Pseudomonas aeruginosa. J. Herpetol. 26, 490-495

S25 Lefcort, H. and Blaustein, A.R. (1995) Disease, predator avoidance, and vulnerability to predation in tadpoles. Oikos 74, 469-474

S26 Romansic, J.M. et al. (2006) Effects of nitrate and the pathogenic water mold Saprolegnia on survival of amphibian larvae. Dis. Aquat. Org. 68, 235-243

S27 Kiesecker, J.M. and Blaustein, A.R. (1995) Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proc. Natl. Acad. Sci. USA 92, 11049-11052

S28 Kiesecker, J.M. and Skelly, D.K. (2001) Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology 82, 1956-1963

S29 Rojas, S. et al. (2005) Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Dis. Aquat. Org. 63, 95–100

S30 Gulland, F.M.D. (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105, 493-503

S31 Murray, D.L. et al. (1997) Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. J. Anim. Ecol. 66, 250-264

S32 Coors, A. et al. (2008) Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 117, 1840-1846

S33 Coors, A. and De Meester, L. (2008) Synergistic, antagonistic and additive effects of multiple stressors: Predation threat, parasitism and pesticide exposure in Daphnia magna. J. Appl. Ecol. 45, 1820-1828

S34 Brown, A.F. and Pascoe, D. (1989) Parasitism and host sensitivity to cadmium: An acanthocephalan infection of the freshwater amphipod Gammarus pulex. J. Appl. Ecol. 26, 473-483

S35 McCahon, C.P. and Poulton, M.J. (1991) Lethal and sub-lethal effects of acid, aluminium and lime on Gammarus pulex during repeated simulated episodes in a Welsh stream. Freshw. Biol. 25, 169-178

S36 Anderson, R.S. et al. (1996) Enhancement of Perkinsus marinus disease progression in TBT-exposed oysters (Crassostrea virginica). Mar. Environ. Res. 42, 177-180

S37 Fisher, W.S. et al. (1999) Decreased resistance of eastern oysters (Crassostrea virginica) to protozoan pathogen (Perkinsus marinus) after sublethal exposure to tributyltin oxide. Mar. Environ. Res. 47, 185-201

S38 Abd Allah, A.T. et al. (1997) Effects of heavy metals on survival and growth of Biomphalaria glabrata Say (Gastropoda: Pulmonata) and interaction with schistosome infection. J. Moll. Stud. 63, 79-86

S39 Guth, D.J. et al. (1977) Potentiation of zinc stress caused by parasitic infection of snails. Hydrobiologia 55, 225-229

S40 Morley, N.J. et al. (2003) Cadmium toxicity and snail- digenean interactions in a population of Lymnaea spp. J. Helminthol. 77, 49-55

S41 Bruno, J.F. et al. (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 6, 1056-1061

S42 Pascoe, D. and Cram, P. (1977) The effect of parasitism on the toxicity of cadmium to the three-spined stickleback, Gasterosteus aculeatus L. J. Fish Biol. 10, 467-472

S43 Moles, A. (1980) Sensitivity of parasitized coho salmon fry to crude oil, toluene, and naphthalene. Trans. Am. Fish. Soc. 109, 293-297

S44 Iwama, G.K. and Greer, G.L. (1980) Effect of bacterial infection on the toxicity of sodium pentachlorophenate to juvenile coho salmon. Trans. Am. Fish. Soc. 109, 290-292

S45 Boyce, N.P. and Yamada, Y. (1977) Effects of a parasite, Eubothrium salvelini (Cestoda: Pseudophyllidea), on the resistance of juvenile sockeye salmon, Oncorhynchus nerka, to zinc. J. Fish. Res. Board Can. 34, 706-709

S46 Prabakaran, M. et al. (2006) Immune response and disease resistance of Oreochromis mossambicus to Aeromonas hydrophila after exposure to hexavalent chromium. Dis. Aquat. Org. 68. 189-196

S47 Fatima, M. et al. (2007) Combined effects of herbicides on biomarkers reflecting immune-endocrine interactions in goldfish Immune and antioxidant effects. Aquat. Toxicol. 81, 159-167.

S48 Khan, R.A. (1987) Effects of chronic exposure to petroleum hydrocarbons on two species of marine fish infected with a hemoprotozoan, Trypanosoma murmanensis. Can. J. Zool. 65, 2703-2709

S49 Gheorgiu, C. et al. (2006) Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata). Parasitology 132, 225-232

S50 Khan, R.A. (1991) Influence of concurrent exposure to crude oil and infection with Trypanosoma murmanensis (Protozoa: Mastigophora) on mortality in winter flounder, Pseudopleuronectes americanus. Can. J. Zool. 69, 876-880

S51 Kelly, D.W. et al. (2009) Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. J. Appl. Ecol. 47, 498-504

S52 Taylor, S.K. et al. (1999) effects of malathion on disease susceptibility in Woodhouse’s toads. J. Wildl. Dis. 35, 536-541

S53 Kerby, J.L. and Storfer, A. (2009) Combined effects of atrazine and chlorpyrifos on susceptibility of the tiger salamander to Ambystoma tigrinum virus. EcoHealth 6, 91-98

S54 Daoust, P.-Y. et al. (1998) Interactive mortality factors in common loons from Maritime Canada. J. Wildl. Dis.34, 524-531

S55 Larsen, M.H. and Mouritsen, K.N. (2009) Increasing temperature counteracts the impact of parasitism on periwinkle consumption. Mar. Ecol. Prog. Ser. 383, 141-149

S56 Hégaret, H. et al. (2009) Perkinsosis in the Manila clam Ruditapes philippinarum affects responses to the harmful-alga, Prorocentrum minimum. J. Exp. Mar. Biol. Ecol. 371, 112-120

S57 Lester, S.E. et al. (2007) Disease dynamics and the potential role of thermal stress in the sea urchin, Strongylocentrotus purpuratus. Can. J. Fish. Aquat. Sci. 64, 314-323

S58 Mitchell, S.E. et al. (2005) Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59, 70-80.

S59 Gollock, M.J. et al. (2005) Physiological responses to acute temperature increase in European eels Anguilla anguilla infected with Anguillicola crassus. Dis. Aquat. Org. 64, 223-228

S60 Koprivnikar, J. et al. (2008) Larval amphibian growth and development under varying density: Are parasitized individuals poor competitors? Oecologia 155, 641-649

S61 Parris, M.J. and Cornelius, T.O. (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85, 3385-3395

S62 Parris, M.J. and Beaudoin, J.G. (2004) Chytriodiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140, 626-632

S63 Johnson, P.T.K. et al. (2006) Adding infection to injury: Synergistic effects of predation and parasitism on amphibian malformations. Ecology 87, 2227-2235

S64 Oppliger, A. et al. (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol. Lett. 1, 129-138

S65 Ould, P., and Welch, H.E. (1980) The effect of stress on the parasitism of mallard ducklings by Echinuria uncinata (Nematoda: Sprirurida). Can. J. Zool. 58, 228-234

S66 Kristen, D.M. and Hammond, K.A. (2000) Combined effects of cold exposure and sub-lethal intestinal parasites on host morphology and physiology. J. Exp. Biol. 203, 3495-3504

S67 Kristen, D.M. and Hammond, K.A. (2001) Parasite infection and caloric restriction induce physiological and morphological plasticity. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 281, R502-R510

S68 Minguez, L. et al. (2009) Interactions between parasitism and biological responses in zebra mussels (Dreissena polymorpha): Importance in ecotoxicological studies. Environ. Res. 109, 843-850

S69 Heinonen, J. et al. (2001) Temperature- and parasite-induced changes in toxicity and lethal body burdens of pentachlorophenol in the freshwater clam Pisidium amnicum. Environ. Toxicol. Chem. 20, 2778-2784

S70 Heinonen, J. et al. (2003) Sublethal energetic responses by Pisidium amnicum (Bivalvia) exposed to pentachlorophenol at two temperatures. Environ. Toxicol. Chem. 22, 433-438

S71 Baudrimont, M. and de Montaudouin, X. (2007) Evidence of an altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule). Parasitology 134, 237-245

S72 Sures, B. and Radszuweit, H. (2007) Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala). J. Helminthol. 81, 191-197

S73 Ruane, N.M. et al. (1999) Modulation of the response of rainbow trout (Oncorhynchus mykiss Walbaum) to confinement, by an ectoparasitic (Argulus foliaceus L.) infestation and cortisol feeding. Fish Physiol. Biochem. 20, 43-51

S74 Ruane, N.M. et al. (2000) Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Krøyer) influences the physiological response to an acute stressor. Fish Shellf. Immunol. 10, 451-463

S75 Blanar, C.A. et al. (2005) Growth, nutritional composition, and hematology of Arctic charr (Salvelinus alpinus) exposed to toxaphene and tapeworm (Diphyllobothrium dendriticum) larvae. Arch. Environ. Contam. Toxicol. 48, 397-404

S76 Schabuss, M. et al. (2005) Ligula intestinalis infection as a potential source of bias in the bioindication of endocrine disruption in the European chub Leuciscus cephalus. J. Helminthol. 79, 91-94

S77 Schuwerack, P.-M.M. et al. (2001) Ammonia-induced cellular and immunological changes in juvenile Cyprinus carpio infected with the blood fluke Sanguinicola inermis. Parasitology 122, 339-345

S78 Hoole, D. et al. (2003) Inflammatory interactions in fish exposed to pollutants and parasites: A role for apoptosis and C reactive protein. Parasitology 126, S71-S85

S79 Dautremepuits, C. et al. (2004) Humoral immune factors modulated by copper and chitosan in healthy or parasitised carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Aquat. Toxicol. 68, 325-338

S80 Dautremepuits, C. et al. (2004) Antioxidant response modulated by copper in healthy or parasitized carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Biochim. Biophys. Acta 1573, 4-8

S81 Gollock, M.J. et al. (2004) The effect of parasitism of European eels with the nematode, Anguillicola crassus on the impact of netting and aerial exposure. Aquaculture 233, 45-54

S82 Sures, B. et al. (2006) Effects of infection with Anguillicola crassus and simultaneous exposure with Cd and 3,3’,4,4’,5-pentachlorobiphenyl (PCB 126) on the levels of cortisol and glucose in European eel (Anguilla anguilla). Parasitology 132, 281-288

S83 Sakanari, J.A. et al. (1984) Effect of sublethal concentrations of zinc and benzene on striped bass, Morone saxatilis (Walbaum), infected with larval Anisakis nematodes. J. Fish Biol. 24, 53-563

S84 Shaw, J.C. et al. (2009) Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc. R. Soc. Ser. B 276, 1137-1146

S85 Marcogliese, D.J. et al. (2005) Joint effects of parasitism and pollution on biomarkers of oxidative stress in yellow perch (Perca flavescens). Dis. Aquat. Org. 63, 77-84

S86 Marcogliese, D.J. et al. (2010) Interactions between parasites and pollutants in yellow perch (Perca flavescens) in the St. Lawrence River, Canada: Implications for resistance and tolerance to parasites. Can. J. Zool. 88, 247-258

S87 Thilakaratne, I.D.S.I.P. et al. (2007) The effects of pollution and parasites on biomarkers of fish health in spottail shiners Notropis hudsonius (Clinton). J. Fish Biol. 71, 519-538

S88 Chivers, D.P. et al. (2007) Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: Possible defence against pathogens, parasites and UVB radiation. Proc. R. Soc. Ser. B 274, 2611-2619

S89 Parris, M.J. and Baud, D.R. (2004) Interactive effects of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysoscelis). Copeia 2004, 344-350.

S90 Kiesecker, J.M. (2002) Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature? Proc. Natl. Acad. Sci. USA 99, 9900-9904

S91 Christin, M.S. et al. (2003) Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ. Toxicol. Chem. 22, 1127-1133

S92 Marcogliese, D.J. et al. (2009) Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catasbeiana. Aquat. Toxicol. 91, 126-134



S93 Sures, B. et al. (2002) Interaction between cadmium exposure and infection with the intestinal parasite Moniliformis moniliformis (Acanthocephala) on the stress hormone levels in rats. Environ. Poll. 119, 333-340


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