Torchin et al. – Introduced species
SUPPLEMENTARY WEB INFORMATION (TORCHIN ET AL.)
EXAMPLES OF PARASITES AND INTRODUCED SPECIES
Most parasites of introduced species were parasites of native hosts that colonized introduced hosts.
These parasites reached prevalences similar to parasites that were introduced from the native range of
the invading host. For example, introduced populations of the mallard duck, Anas platyrhynchos, were
infected with 31 parasite species. Of these, 21 do not occur in the duck’s native range. Additionally,
the mean prevalence of the native parasites that colonized introduced populations was 12% compared
to 10% for those that derived from the native range of the duck.
Introduced hosts may become sinks for some native parasites if they are insufficiently adapted to the
novel hosts to complete their development. Some of these maladapted parasites can cause substantial
pathology in their new hosts. As an example, the striped bass, Morone saxatilis, was introduced from
the eastern U.S.A. to the San Francisco Bay delta, where it became commonly infected by larval stages
of the tapeworm, Lacistorhynchus dollfusi 1. The parasite elicits a strong immune response in the host,
preventing its further development but also harming the fish. Such maladaptions may diminish over
time due to natural selection. This was demonstrated by Sakanari and Moser2 who experimentally
infected striped bass from San Francisco Bay as well as naïve bass from native Atlantic populations.
They found that fish from naïve native populations had higher intensity infections and elicited a much
stronger immune response, resulting in more tissue damage to the fish.
The likelihood that a parasite will encounter and shift to an introduced species may change over time,
as will the potential for a parasite to evolve the ability to utilize a novel (introduced) host. This is
supported by the positive association between parasite colonization on an invader and time since
invasion3-5. Additionally, we surmise that species that invade regions with phylogenetically and
ecologically similar species will experience higher rates of parasitization by native parasites than will
hosts that became established in areas without similar species. Similarly, the larger the new
geographic range of the invader, the more parasites it is likely to encounter6.
CRITERIA FOR SELECTING STUDIES
We generated a list of species for the analysis using a stratified random procedure designed to
minimize biases associated with non-random selection. First, we identified lists of invasive species for
particular geographic regions7-11. We then conducted a literature search of all species listed in these
references using Biological Abstracts (1985-2001, online versions) using genus, species and parasit# or
infect# or pathogen# as keywords. We selected host species where this search revealed ten or more
citations, or those, which we knew had been parasitologically examined. For taxa that had over ten
species which fit these criteria, we randomly selected ten species and continued our search. From this
list, we compiled parasitological data from any available source. Several of these had been sufficiently
studied to provide prevalence data in both the native and introduced ranges of the invader. We
excluded studies focusing on a single parasite species. We also excluded host species under culture
from our comparison because these species are introduced intentionally, are managed to reduce
parasitism and are typically grown at unnaturally high densities which promotes disease transmission.
As a result of our search strategy, for amphibians, reptiles, birds and mammals, the parasitological
studies used for comparing native and introduced regions were comprised exclusively of parasitic
helminths.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Sakanari, J. A. & Moser, M. Lesion induction by the plerocercoid Lacistorhynchus tenuis
(Cestoda) and wound healing in the striped bass, Morone saxatilis. Journal of Fish Biology 28,
289-296 (1986).
Sakanari, J. A. & Moser, M. Adaptation of an introduced host to an indigenous parasite.
Journal of Parasitology 76, 420-423 (1990).
Blaustein, A. R., Kuris, A. M. & Alió, J. J. Pest and parasite species-richness problems.
American Naturalist 122, 556-566 (1983).
Cornell, H. V. & Hawkins, B. A. in Parasitoid Community Ecology (eds. Hawkins, B. A. &
Sheehan, W.) 77-89 (Oxford University Press, Oxford, 1994).
Guegan, J. F. & Kennedy, C. R. Maximum local helminth parasite community richness in
British freshwater fish: A test of the colonization time hypothesis. Parasitology 106, 91-100
(1993).
Combes, C. Parasitism: the ecology and evolution of intimate interactions (ed. Thompson, J.
N.) (University of Chicago Press, Chicago, 2001).
CIESM. Atlas of exotic species in the Mediterranean Sea
http://www.ciesm.org/atlas/index/html., (2001).
Ruiz, G. M., Fofonoff, P., Carlton, J. T., Wonham, M. J. & Hines, A. H. Invasions of coastal
marine communities in North America: apparent patterns, processes, and biases. Ann. Rev.
Ecol. Syst. 31, 481-531 (2000).
Smith, H. M. & Kohler, A. J. A survey of herpetological introductions in the United States and
Canada. Transactions of the Kansas Academy of Science 80, 1-24 (1978).
USGS. US Geological Survey Nonindigenous Aquatic Species http://nas.er.usgs.gov., (2001).
Contreras-B, S. & Escalante-C., M. A. in Distribution, biology, and management of exotic
fishes
(eds. Courtenay, W. R. & Stauffer, J. R.) 103-130 (Johns Hopkins University Press, Baltimore,
1984).
SUPPLEMENTARY TABLE I: PARASITE DATA COLLECTION FOR 26 HOST SPECIES
Table of host species used in our comparison of parasites in native and introduced* regions.
*References with asterisks indicate introduced host populations.
Host Taxon
Molluscs
Host Species
Batillaria cumingii
References
Harada and Suguri, 1989; Rybakov and Lukomskaya, 1986; Shimura and
Ito, 1980; *Ching, 1991; *Torchin et al. (in review); *Whitlatch, 1974
Molluscs
Bythinia tentaculata
Mattison et al., 1995; Probert, 1966; Toledo et al., 1998; *Lepitski and Scott,
1994; *Lepitski et al., 1994, *Ménard and Scott, 1987
Molluscs
Dreissena polymorpha
Burlakova et al., 1998; Molloy et al., 1996; Wallet et al., 1985; *Conn and
Conn, 1995; *Conn et al., 1996; *Toews et al., 1993
Molluscs
Ilyanassa obsoleta
Curtis, 1997; Curtis and Hubbard, 1990; Stambaugh and McDermott, 1969;
*Grodhaus and Keh, 1958
Molluscs
Littorina littorea
Hughes and Answer, 1982; Huxham et al., 1993; Lauckner, 1987; Matthews
et al., 1985; Williams and Ellis, 1975; *Hoff, 1941; *Pohley, 1976
Molluscs
Melanoides tuberculata
Ismail and Abdel-Hafez, 1987; Ismail and Arif, 1993; *Mitchell et al., 2000;
*Salgado-Maldonado, 1995
Molluscs
Potamopyrgus antipodarum Winterbourn, 1973; *Fretter and Graham, 1962; *Torchin (unpub. data)
Crustaceans
Carcinus maenas
*Brattey et al., 1985; *Torchin et al., 2001
Crustaceans
Cancer novaezelandiae
Kuris and Gurney, 1997; Torchin et al., 2002b
Crustaceans
Hemigrapsus sanguineus
Yamaguchi et al., 1994; *McDermott, 1998; *Torchin et al., 2002a
Fishes
Gambusia affinis
Davis and Huffman, 1977; Davis and Huffman, 1978; Marcogliese and
Esch, 1989; Overstreet, 1997; Winemiller and Winsborough, 1990;
*Dove, 2000; *Torres et al., 1991
Fishes
Onchorynchus mykiss
Bortz et al., 1988; Ching, 1985; Kabata and Whitaker, 1989; *Kennedy
et al., 1986; *Poynton, 1986; *Weekes and Penlington, 1986
Fishes
Perca fluviatilis
Halmetoja et al., 2000; Lucky and Navrátil, 1984; *Dove, 1999
Fishes
Pimephales promelas
Dick, 1987; Dick et al., 1987; Marcogliese, 1991; Smith, 1986; *Brouder
and Hoffnagle, 1997; *Clarkson et al., 1997
Fishes
Poecilia lattipinna
Hoffman, 1999; *Torchin (unpub. data)
Fishes
Poecilia reticulata
Harris and Lyles, 1992; Lyles, 1990; *Dove and Ernst, 1998; *Font and
Tate, 1994
Amphibians
Bufo marinus
Galicia-Guerrero et al., 2000; McKenzie, 2000; *Barton and Pichelin, 1999;
*Goldberg and Bursey, 1992; *Goldberg et al., 1995
Amphibians
Rana catesbeiana
Andrews et al., 1992; Bursey and DeWolf, 1998; McAlpine, 1997; *Goldberg
et al., 1998; *Oyamada et al., 1998
Reptiles
Lepidodactylus lugubris
Bursey and Goldberg, 2001; Goldberg et al., 1998;Goldberg et al., 2000;
Hanley et al., 1995; *Goldberg and Bursey, 1997
Birds
Anas platyrhynchos
Islam et al., 1988; Kulisic and Lepojev, 1994; *Eom et al., 1984; *Farias
and Canaris, 1986; *Shaw and Kogan, 1980
Birds
Passer domesticus
Borgsteede et al., 2000; Joszt, 1962; *Brasil and Amato, 1992; *Cooper
and Crites, 1974; *Cooper and Crites, 1976; *Hopkins and Wheaton, 1935
Birds
Sturnus vulgaris
Borggsteede et al., 2000; Gundlach, 1965; James and Llewellyn, 1967;
Owen and Pemberton, 1962; *Boyd, 1951; *Carter et al., 1973; *Cooper
and Crites, 1975; *Cooper and Crites, 1976; *Vincent, 1972
Mammals
Oryctolagus cuniculus
Mammals
Rattus rattus
Mammals
Trichosurus vulpecula
Mammals
Vulpes vulpes
Allan et al., 1999; Blasco et al.,1996; Boag, 1985; 1987;1988; Boag and
Iason, 1986; Boag and Kolb, 1989; Butler, 1994; Molina et al., 1998; *Bull,
1964; *Casanova et al., 1996; *Dudzinski and Mykytowycz, 1963;
*Dunsmore and Dudzinski, 1968; *Hobbs et al., 1999; *Pisano et al., 2001
Hasegawa et al., 1994; Hasegawa and Syafruddin, 1995; Huq et al., 1985;
Mafiana et al., 1997; Casanova et al., 1996; *Miquel et al., 1996;
*Pisano et al., 2001
O'Callaghan and Moore, 1986; Presidente et al., 1982; *Stankiewicz
et al., 1998
Criado-Fornelio et al., 2000; Deblock et al., 1988; Hofer et al., 2000;
Papadopoulos et al., 1997; Richards et al., 1995; *Coman, 1973;
*Conti, 1984; *Davidson et al., 1992; El-Shehabi et al., 1999; *Ryan,
1976; *Sato et al., 1999
SUPPLEMENTARY TABLE I REFERENCES:
In alphabetical order
1.
2.
3.
4.
5.
6.
7.
8.
9.
Allan, J. C. et al. Helminth parasites of the wild rabbit Oryctolagus cuniculus near Malham
Tarn, Yorkshire, UK. Journal of Helminthology. 73, 289-294 (1999).
Andrews, K. D. et al. Helminths of Rana-Catesbeiana in Southern Illinois with A Checklist of
Helminths in Bullfrogs of North America. Transactions of the Illinois State Academy of Science
85, 147-172 (1992).
Barton, D. P. & Pichelin, S. Acanthocephalus bufonis (Acanthocephala) from Bufo marinus
(Bufonidae: Amphibia) in Hawaii. Parasite 6, 269-272 (1999).
Blasco, S. et al. The helminthfauna of Oryctolagus cuniculus (Linnaeus, 1758) in the Iberian
Peninsula. Faunistic and ecological considerations. Parasite 3, 327-333 (1996).
Boag, B. The incidence of helminth parasites from the wild rabbit Oryctolagus cuniculus in
Eastern Scotland [UK]. Journal of Helminthology 59, 61-69 (1985).
Boag, B. The Helminth Parasites of the Wild Rabbit Oryctolagus-Cuniculus and the Brown
Hare Lepus-Capensis from the Isle of Coll Scotland Uk. Journal of Zoology (London) 212,
352-355 (1987).
Boag, B. Observations on the seasonal incidence of myxomatosis and its interactions with
helminth parasites in the European rabbit (Oryctolagus cuniculus). Journal of Wildlife Diseases
24, 450-455 (1988).
Boag, B. & Iason, G. The occurrence and abundance of helminth parasites of the mountain hare
Lepus timidus and the wild rabbit Oryctolagus cuniculus in Aberdeenshire, Scotland [UK].
Journal of Helminthology 60, 92-98 (1986).
Boag, B. & Kolb, H. H. Influence of host age and sex on nematode populations in the wild
rabbit (Oryctolagus cuniculus L.). Proceedings of the Helminthological Society of Washington
56, 116-119 (1989).
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
Borgsteede, F. H. M., Okulewicz, A. & Okulewicz, J. A study of the helminth fauna of birds
belonging to the Passeriformes in the Netherlands. Acta Parasitologica 45, 14-21 (2000).
Bortz, B. M., Kenny, G. E., Pauley, G. B. & Bunt-Milam, A. H. Prevalence of two site-specific
populations of Diplostomum spp. in eye infections of rainbow trout, Salmo gairdneri
Richardson, from lakes in Washington State, USA. Journal of Fish Biology 33, 31-44 (1988).
Boyd, E. M. A survey of parasitism of the starling Sturnus vulgaris L. in North America.
Journal of Parasitology 37, 56-84 (1951).
Brasil, M. D. C. & Amato, S. B. Faunistic Analysis of the Helminths of Sparrows Passerdomesticus L. 1758 Captured in Campo Grande Rio de Janeiro Rj. Memorias do Instituto
Oswaldo Cruz Rio de Janeiro 87, 43-48 (1992).
Brattey, J., Elner, R. W., Uhazy, L. S. & Bagnall, A. E. Metazoan parasites and commensals of
five crab (Brachyura) species from eastern Canada. Canadian Journal of Zoology 63, 22242229 (1985).
Brouder, M. J. & Hoffnagle, T. L. Distribution and prevalence of the Asian fish tapeworm,
Bothriocephalus acheilognathi, in the Colorado River and tributaries, Grand Canyon, Arizona,
including two new host records. Journal of the Helminthological Society of Washington 64,
219-226 (1997).
Bull, P. C. Ecology of helminth parasites of the wild rabbit (Oryctolagus cuniculus L.) in New
Zealand. New Zealand Dept. of Scientific and Industrial Research Bulletin 158, 1-147 (1964).
Burlakova, L. E., Karatayev, A. Y. & Molloy, D. P. Field and laboratory studies of zebra
mussel (Dreissena polymorpha) infection by the ciliate Conchophthirus acuminatus in the
Republic of Belarus. Journal of Invertebrate Pathology 71, 251-257 (1998).
Bursey, C. R. & Dewolf, W. F., II. Helminths of the frogs, Rana catesbeiana, Rana clamitans,
and Rana palustris, from Coshocton County, Ohio. Ohio Journal of Science 98, 28-29 (1998).
Bursey, C. R. & Goldberg, S. R. Physalopteroides arnoensis n. sp. (Nematoda:
Physalopteroidea) and other intestinal helminths of the mourning gecko, Lepidodactylus
lugubris (Sauria: Gekkonidae), from Arno Atoll, Republic of the Marshall Islands, Oceania.
Journal of Parasitology 87, 135-138 (2001).
Butler, F. T. Arthropod and helminth parasites from rabbits Oryctolagus cuniculus in southwest Ireland. Irish Naturalists' Journal 24, 392-395 (1994).
Carter, J. M., Canaris, A. G. & Bristol, J. R. A survey of the parasites of starlings (Sturnus
vulgaris L.) in El Paso County, Texas. Journal of Parasitology 59, 775 (1973).
Casanova, J. C. et al. On the helminthfauna of wild mammals (Rodentia, Insectivora and
Lagomorpha) in Azores Archipelago (Portugal). Vie et Milieu 46, 253-259 (1996).
Ching, H. L. Occurrence of the eyefluke, Diplostomum baeri bucculentum in salmonid fishes of
northern British Columbia [Canada]. Canadian Journal of Zoology 63, 396-399 (1985).
Ching, H. L. Lists of larval worms from marine invertebrates of the Pacific Coast of North
America. Journal of the Helminthological Society of Washington 58, 57-68 (1991).
Clarkson, R. W., Robinson, A. T. & Hoffnagle, T. L. Asian tapeworm (Bothriocephalus
acheilognathi) in native fishes from the Little Colorado River, Grand Canyon, Arizona. Great
Basin Naturalist 57, 66-69 (1997).
Coman, B. J. Helminth parasites of the fox (Vulpes vulpes) in Victoria. Australian Veterinary
Journal 49, 378-384 (1973).
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
Conn, D. B. & Conn, D. A. Experimental infection of zebra mussels Dreissena polymorpha
(Mollusca: Bivalvia) by metacercariae of Echinoparyphium sp. (Platyhelminthes: Trematoda).
Journal of Parasitology 81, 304-305 (1995).
Conn, D. B., Ricciardi, A., Babapulle, M. N., Klein, K. A. & Rosen, D. A. Chaetogaster
limnaei (Annelida: Oligochaeta) as a parasite of the zebra mussel Dreissena polymorpha, and
the quagga mussel Dreissena bugensis (Mollusca: Bivalvia). Parasitology Research 82, 1-7
(1996).
Conti, J. A. Helminths of Foxes and Coyotes Canis-latrans in Florida Usa. Proceedings of the
Helminthological Society of Washington 51, 365-367 (1984).
Contreras-B, S. & Escalante-C, M. A. in Distribution, biology, and management of exotic fishes
(eds. Courtenay, W. R. J. & Stauffer, J. R. J.) (John Hopkins University Press, Baltimore,
1984).
Cooper, C. L. & Crites, J. L. Helminth parasitism in juvenile house sparrows, Passer
domesticus (L.), from South Bass Island, Ohio, including a list of helminths reported from this
host in North America. Ohio Journal of Science 74, 388-389 (1974).
Cooper, C. L. & Crites, J. L. Helminths parasites of the starling (Sturnus vulgaris L.) from
South Bass Island, Ohio. Journal of Parasitology 61, 161 (1975).
Cooper, C. L. & Crites, J. L. Community ecology of helminth parasitism in an insular passerine
avifauna. Journal of Parasitology 62, 105-110 (1976).
Criado-Fornelio, A. et al. A parasitological survey of wild red foxes (Vulpes vulpes) from the
province of Guadalajara, Spain. Veterinary Parasitology 92, 245-251 (2000).
Curtis, L. A. Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries.
Journal of Parasitology 83, 793-803 (1997).
Curtis, L. A. & Hubbard, K. M. Trematode infections in a gastropod host misrepresented by
observing shed cercariae. Journal of Experimental Marine Biology and Ecology 143, 131-138
(1990).
Davidson, W. R., Appel, M. J., Doster, G. L., Baker, O. E. & Brown, J. F. Diseases and
Parasites of Red Foxes Gray Foxes and Coyotes from Commercial Sources Selling To FoxChasing Enclosures. Journal of Wildlife Diseases 28, 581-589 (1992).
Davis, J. R. & Huffman, D. G. A comparison of the helminth parasites of Gambusia affinis and
Gambusia geiseri (Osteichthys: Poeciliidae) from the Upper San Marcos River. Southwestern
Naturalist 22, 359-366 (1977).
Davis, J. R. & Huffman, D. G. Some factors associated with the distribution of helminths
among individual mosquitofish, Gambusia affinis. Texas Journal of Science 30, 43-53 (1978).
Deblock, S., Petavy, A. F. & Gilot, B. Intestinal helminths of the red fox (Vulpes vulpes L.) in
the Massif Central, France. Canadian Journal of Zoology 66, 1562-1569 (1988).
Dick, T. A. The atrium of the fish heart as a site for Contracaecum spp. larvae. Journal of
Wildlife Diseases 23, 328-330 (1987).
Dick, T. A., Papst, M. H. & Paul, H. C. Rainbow trout (Salmo gairdneri) stocking and
Contracaecum spp. Journal of Wildlife Diseases 23, 242-247 (1987).
Dove, A. D. M. in Department of Microbiology and Parasitology 280 (The University of
Queensland, Queensland, 1999).
Dove, A. D. M. Richness patterns in the parasite communities of exotic poeciliid fishes.
Parasitology 120, 609-623 (2000).
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
Dove, A. D. M. & Ernst, I. Concurrent invaders: Four exotic species of Monogenea now
established on exotic freshwater fishes in Australia. International Journal for Parasitology 28,
1755-1764 (1998).
Dudzinski, M. L. & Mykytowycz, R. Relationship between sex and age of rabbits, Oryctolagus
cuniculus (L.) and infection with nematodes Trichostrongylus retortaeformis and Graphidium
strigosum. Journal of Parasitology 49, 55-59 (1963).
Dunsmore, J. D. & Dudzinski, M. L. Relationship of numbers of nematode parasites in wild
rabbits, Oryctolagus cuniculus (L.), to host sex, age, and season. Journal of Parasitology 54,
462-474 (1968).
El-Shehabi, F. S., Abdel-Hafez, S. K. & Kamhawi, S. A. Prevalence of intestinal helminths of
dogs and foxes from Jordan. Parasitology Research 85, 928-934 (1999).
Eom, K. S., Rim, H. J. & Jang, D. H. A study on the parasitic helminths of domestic duck
(Anas platyrhynchos var. domestica) in Korea. Korean Journal of Parasitology 22, 215-221
(1984).
Farias, J. D. & Canaris, A. G. Gastrointestinal helminths of the Mexican duck, Anas
platyrhynchos diazi, from north central Mexico and southwestern USA. Journal of Wildlife
Diseases 22, 51-54 (1986).
Font, W. F. & Tate, D. C. Helminth parasites of native Hawaiian freshwater fishes: An example
of extreme ecological isolation. Journal of Parasitology 80, 682-688 (1994).
Fretter, V. & Graham, A. British Prosobranch Molluscs (Ray Society, London, 1962).
Galicia-Guerrero, S., Bursey, C. R., Goldberg, S. R. & Salgado-Maldonado, G. Helminths of
two sympatric toad species, Bufo marinus (Linnaeus) and Bufo marmoreus Wiegmann, 1833
(Anura: Bufonidae) from Chamela, Jalisco, Mexico. Journal of the Helminthological Society of
Washington 67, 129-133 (2000).
Goldberg, S. R. & Bursey, C. R. Helminths of the marine toad, Bufo marinus (Anura:
Bufonidae), from American Samoa. Journal of the Helminthological Society of Washington 59,
131-133 (1992).
Goldberg, S. R. & Bursey, C. R. New helminth records for the mourning gecko, Lepidodactylus
lugubris (Gekkonidae) from Hawaii. Bishop Museum Occasional Papers 0, 54-56 (1997).
Goldberg, S. R., Bursey, C. R. & Cheam, H. Helminths of two native frog species (Rana
chiricahuensis, Rana yavapaiensis) and one introduced frog species (Rana catesbeiana)
(Ranidae) from Arizona. Journal of Parasitology 84, 175-177 (1998).
Goldberg, S. R., Bursey, C. R. & Cheam, H. Gastrointestinal helminths of four gekkonid
lizards, Gehyra mutilata, Gehyra oceanica, Hemidactylus frenatus and Lepidodactylus lugubris
from the Mariana Islands, Micronesia. Journal of Parasitology 84, 1295-1298 (1998).
Goldberg, S. R., Bursey, C. R. & Cheam, H. Gastrointestinal helminths of four lizard species
from Moorea, French Polynesia. Journal of the Helminthological Society of Washington 67,
118-121 (2000).
Goldberg, S. R., Bursey, C. R. & Tawil, R. Helminths of an Introduced Population of the Giant
Toad, Bufo marinus (Anura: Bufonidae), from Bermuda. Journal of the Helminthological
Society of Washington 62, 64-67 (1995).
Granovitch, A. I., Sergievsky, S. O. & Sokolova, I. M. Spatial and temporal variation of
trematode infection in coexisting populations of intertidal gastropods Littorina saxatilis and L.
obtusata in the White Sea. Diseases of Aquatic Organisms 41, 53-64 (2000).
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
76.
77.
Grodhaus, G. & Keh, B. The marine, dermatitus-producing cercaria of Austrobilharzia
variglandis in California (Trematoda: Schistosomatidae). Journal of Parasitology 44, 633-638
(1958).
Gundlach, J. L. The helminth parasites of the starling (Sturnus vulgaris L.) of the Lublin
Palatinate. Acta Parasitologica Polonica 13, 215-225 (1965).
Halmetoja, A., Valtonen, E. T. & Koskenniemi, E. Perch (Perca fluviatilis L.) parasites reflect
ecosystem conditions: A comparison of a natural lake and two acidic reservoirs in Finland.
International Journal for Parasitology 30, 1437-1444 (2000).
Hanley, K. A., Vollmer, D. M. & Case, T. J. The distribution and prevalence of helminths,
coccidia and blood parasites in two competing species of gecko: Implications for apparent
competition. Oecologia (Berlin) 102, 220-229 (1995).
Harada, M. & Suguri, S. Surveys on cercariae in brackish water snails in Kagawa Prefecture,
Shikoku, Japan. Japanese Journal of Parasitology 38, 388-391 (1989).
Harris, P. D. & Lyles, A. M. Infections of Gyrodactylus bullatarudis and Gyrodactylus
turnbulli New-Record on Guppies Poecilia reticulata in Trinidad. Journal of Parasitology 78,
912-914 (1992).
Hasegawa, H., Kobayashi, J. & Otsuru, M. Helminth parasites collected from Rattus rattus on
Lanyu, Taiwan. Journal of the Helminthological Society of Washington 61, 95-102 (1994).
Hasegawa, H. & Syafruddin. Nematode Fauna of the Two Sympatric Rats Rattus rattus and R.
exulans, in Kao District, Halmahera Island, Indonesia. Journal of the Helminthological Society
of Washington 62, 27-31 (1995).
Hobbs, R. P., Twigg, L. E., Elliot, A. D. & Wheeler, A. G. Factors influencing the fecal egg
and oocyst counts of parasites of wild European rabbits Oryctolagus cuniculus (L.) in southern
western Australia. Journal of Parasitology 85, 796-802 (1999).
Hofer, S. et al. High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes
vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120,
135-142 (2000).
Hoff, C. C. A case of correlation between infection of snail hosts with Cryptocotyle lingua and
the habits of gulls. Journal of Parasitology 27, 539 (1941).
Hopkins, S. H. & Wheaton, E. Intestinal parasites of English sparrows in Illinois. Journal of
Parasitology 21, 316-317 (1935).
Hughes, R. N. & Answer, P. Growth, Spawning, and trematode infection of Littorina littorea
(L.) from an exposed shore in North Wales. J. Moll. Stud. 48, 331-341 (1982).
Huq, M. M., Karim, M. J. & Sheikh, H. Helminth parasites of rats, house mice and moles in
Bangladesh. Pakistan Veterinary Journal 5, 143-144 (1985).
Huxham, M., Raffaelli, D. & Pike, A. The influence of Cryptocotyle lingua (Digenea:
Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda:
Prosobranchia): An ecological approach. Journal of Experimental Marine Biology and Ecology
168, 223-238 (1993).
Islam, M. R., Shaikh, H. & Baki, M. A. Prevalence and pathology of helminth parasites in
domestic ducks of Bangladesh. Veterinary Parasitology 29, 73-78 (1988).
Ismail, N. S. & Abdel-Hafez, S. K. Seasonal Variation in Infection Rates of Melanoides
tuberculata Muller Snails with Larval Trematodes in Azraq Jordan. Helminthologia
(Bratislava) 24, 293-301 (1987).
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
92.
93.
94.
Ismail, N. S. & Arif, A. M. S. Population dynamics of Melanoides tuberculata (Thiaridae)
snails in a desert spring, United Arab Emirates and infection with larval trematodes.
Hydrobiologia 257, 57-64 (1993).
James, B. L. Studies on the life cycle of Microphallus pygmaeus (Levinsen, 1888) (Trematoda:
Microphallidae). Journal of Natural History 2, 155-172 (1968).
James, B. L. & Llewellyn, L. C. A quantitative analysis of helminth infestation in some
passerine birds found dead on the island of Skomer. Journal of Helminthology 41, 19-44
(1967).
Joszt, L. Helminth parasites of sparrow - Passer domesticus (L.) in the environment of
Warszawa. Acta Parasitologica Polonica 10, 113-123 (1962).
Kabata, Z., Whitaker, D. J. & Bagshaw, J. W. Kudoa thyrsitis (Myxosporea: Multivalvulida) in
coho salmon, Oncorhynchus kisutch. Canadian Journal of Zoology 64, 1038-1040 (1986).
Kennedy, C. R., Laffoley, D. D., Bishop, G., Jones, P. & Taylor, M. Communities of parasites
of freshwater fish of Jersey, Channel Islands [UK]. Journal of Fish Biology 29, 215-226
(1986).
Kulisic, Z. & Lepojev, O. Trematodes of wild duck (Anas platyrhynchos L.) in the Belgrade
area. Acta Veterinaria (Belgrade) 44, 323-328 (1994).
Lauckner, G. Ecological Effects of Larval Trematode Infestation on Littoral Marine
Invertebrate Populations. International Journal for Parasitology 17, 391-398 (1987).
Lepitzki, D. A. W., Scott, M. E. & McLaughlin, J. D. Assessing cercarial transmission of
Cyathocotyle bushiensis and Sphaeridiotrema pseudoglobulus by use of sentinel snails.
Canadian Journal of Zoology 72, 885-891 (1994).
Lepitzki, D. A. W., Scott, M. E. & McLaughlin, J. D. Influence of storage and examination
methods on the recovery and size of metacercariae of Cyathocotyle bushiensis and
Sphaeriditotrema pseudoglobulus (Digenea). Journal of Parasitology 80, 454-460 (1994).
Lucky, Z. & Navratil, S. Parasitic diseases of the perch (Perca fluviatilis) in detention
reservoirs of the Morava River Basin [Czechoslovakia]. Acta Veterinaria Brno 53, 81-90
(1984).
Lyles, A. M. in Ecology, Evolution, and Behavior (Princeton University, 1990).
Mafiana, C. F., Osho, M. B. & Sam-Wobo, S. Gastrointestinal helminth parasites of the black
rat (Rattus rattus) in Abeokuta, southwest, Nigeria. Journal of Helminthology 71, 217-220
(1997).
Marcogliese, D. J. Seasonal occurrence of Lernaea cyprinacea on fishes in Belews Lake, North
Carolina, [USA]. Journal of Parasitology 77, 326-327 (1991).
Marcogliese, D. J. & Esch, G. W. Alterations in seasonal dynamics of Bothriocephalus
acheilognathi in a North Carolina [USA] cooling reservoir over a seven-year period. Journal of
Parasitology 75, 378-382 (1989).
Matthews, P. M., Montgomery, W. I. & Hanna, R. E. B. Infestation of littorinids by larval
digenea around a small fishing port. Parasitology 90, 277-288 (1985).
Mattison, R. G., Dunn, T. S., Hanna, R. E. B., Nizami, W. A. & Ali, Q. M. Population
dynamics of freshwater gastropods and epidemiology of their helminth infections with
emphasis on larval paramphistomes in northern India. Journal of Helminthology 69, 125-138
(1995).
95.
96.
97.
98.
99.
100.
101.
102.
103.
104.
105.
106.
107.
108.
109.
110.
McAlpine, D. F. Helminth communities in bullfrogs (Rana catesbeiana), green frogs (Rana
clamitans), and leopard frogs (Rana pipiens) from New Brunswick, Canada. Canadian Journal
of Zoology 75, 1883-1890 (1997).
McAlpine, D. F. & Burt, M. D. B. Helminths of bullfrogs, Rana catesbeiana, green frogs, R.
clamitans, and leopard frogs, R. pipiens in New Brunswick. Canadian Field-Naturalist 112,
50-68 (1998).
McDermott, J. J. The western Pacific brachyuran (Hemigrapsus sanguineus: Grapsidae), in its
new habitat along the Atlantic coast of the United States: Geographic distribution and ecology.
ICES Journal of Marine Science 55, 289-298 (1998).
McKenzie, V. in Dept. of Ecology and Evolutionary Biology 1-156 (University of Connecticut,
Storrs, 2000).
Menard, L. & Scott, M. E. Seasonal occurrence of Cyathocotyle bushiensis Khan, 1962
(Digenea: Cyathocotylidae) metacercariae in the intermediate host Bithynia tentaculata L.
(Gastropoda: Prosobranchia). Canadian Journal of Zoology 65, 2980-2992 (1987).
Miquel, J. et al. Ecological features on the helminth fauna of Muridae species (Rodentia) in
Hyeres Archipelago (Var, France). Vie et Milieu 46, 219-223 (1996).
Mitchell, A. J., Salmon, M. J., Huffman, D. G., Goodwin, A. E. & Brandt, T. M. Prevalence
and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the
fountain darter, in two central Texas spring-fed rivers. Journal of Aquatic Animal Health 12,
283-289 (2000).
Molina, X., Casanova, J. C., Feliu, C. & Castien, E. Studies of wild rabbit (Oryctolagus
cuniculus) populations in Navarra (Spain). III. Qualitative and quantitative composition of the
rabbit parasitic helminthfauna. Gibier Faune Sauvage 15, 123-133 (1998).
Molloy, D. P., Roitman, V. A. & Shields, J. D. Survey of parasites of zebra mussels (Bivalvia:
Dreissenidae) in northwestern Russia, with comments on records of parasitism in Europe and
North America. Journal of the Helminthological Society of Washington 63, 251-256 (1996).
O'Callaghan, M. G. & Moore, E. Parasites and Serological Survey of the Common Brushtail
Possum Trichosurus vulpecula from Kangaroo Island South Australia. Journal of Wildlife
Diseases 22, 589-591 (1986).
Overstreet, R. M. Parasitological data as monitors of environmental health. Parassitologia
(Rome) 39, 169-175 (1997).
Owen, R. W. & Pemberton, R. T. Helminth infection of the starling (Sturnus vulgaris L.) in
northern England. Proceedings of the Zoological Society of London 139, 557-587 (1962).
Oyamada, T. et al. Spontaneous larval Gnathostoma nipponicum infection in frogs. Journal of
Veterinary Medical Science 60, 1029-1031 (1998).
Papadopoulos, H., Himonas, C., Papazahariadou, M. & Antoniadou-Sotiriadou, K. Helminths
of foxes and other wild carnivores from rural areas in Greece. Journal of Helminthology 71,
227-231 (1997).
Pisanu, B., Chapuis, J. L. & Durette-Desset, M. C. Helminths from introduced small mammals
on Kerguelen, Crozet, and Amsterdam Islands (Southern Indian Ocean). Journal of
Parasitology 87, 1205-1208 (2001).
Pohley, W. J. Relationships among three species of Littorina and their larval digenea. Marine
Biology 37, 179-186 (1976).
111.
112.
113.
114.
115.
116.
117.
118.
119.
120.
121.
122.
123.
124.
125.
126.
127.
Poynton, S. L. Distribution of the flagellate Hexamita salmonis and the microsporidian Loma
salmonae in brown trout, Salmo trutta, and rainbow trout, Salmo gairdneri, in the River Itchen
(UK) and three of its fish farms. Journal of Fish Biology 29, 417-430 (1986).
Presidente, P. J. A., Barnett, J. L., How, R. A. & Humphreys, W. F. Effects of habitat, host sex
and age on the parasites of Trichosurus caninus (Marsupiala: Phalangeridae) in North-eastern
New South Wales. Australian Journal of Zoology 30, 33-47 (1982).
Probert, A. J. Studies on the incidence of larval trematodes infecting the freshwater molluscs of
Llangorse Lake, South Wales. Journal of Helminthology 40, 115-130 (1966).
Richards, D. T., Harris, S. & Lewis, J. W. Epidemiological studies on intestinal helminth
parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Veterinary
Parasitology 59, 39-51 (1995).
Ryan, G. E. Helminth parasites of the fox (Vulpes vulpes) in New South Wales. Australian
Veterinary Journal 52, 126-131 (1976).
Rybakov, A. V. & Lukomskaya, O. G. On the life cycle of Acanthoparyphium macracanthum,
new species (Trematoda, Echinostomatidae). Parazitologiya (St. Petersburg) 22, 224-229
(1988).
Salgado-Maldonado, G., Rodriguez-Vargas, M. I. & Campos-Perez, J. J. Metacercariae of
Centrocestus formosanus (Nishigori, 1924) (Trematoda) in freshwater fishes in Mexico and
their transmission by the thiarid snail Melanoides tuberculata. Studies on Neotropical Fauna
and Environment 30, 245-250 (1995).
Sato, H., Inaba, T., Ihama, Y. & Kamiya, H. Parasitological survey on wild carnivora in northwestern Tohoku, Japan. Journal of Veterinary Medical Science 61, 1023-1026 (1999).
Shaw, m. g. & Kogan, a. a. Helminth fauna of waterfowl in Central Oklahoma. Journal of
Wildlife Diseases 16, 59-64 (1980).
Shimura, S. & Ito, J. Two new species of marine cercariae from the Japanese intertidal
gastropod, Batillaria cumingii (Crosse). Japanese Journal of Parasitology 29, 369-375 (1980).
Stambaugh, J. E. & McDermott, J. J. The effects of trematode larvae on the locomotion of
naturally infected Nassarius obsoletus (Gastropoda). Proceedings of the Pa. Academy of
Science 43, 226-231 (1969).
Stankiewicz, M., Cowan, P. E. & Heath, D. D. Endoparasites of possums from selected areas of
North Island, New Zealand. New Zealand Journal of Zoology 25, 91-97 (1998).
Toews, S., Beverley-Burton, M. & Lawrimore, T. Helminth and protist parasites of zebra
mussels, Dreissena polymorpha (Pallas, 1771), in the Great Lakes region of southwestern
Ontario, with comments on associated bacteria. Canadian Journal of Zoology 71, 1763-1766
(1993).
Toledo, R., Munoz-Antoli, C., Perez, M. & Esteban, J. G. Larval trematode infections in
freshwater gastropods from the Albufera Natural Park in Spain. Journal of Helminthology 72,
79-82 (1998).
Torchin, M. E., Byers, J. E. & Huspeni, T. C. Cryptic impacts of invasive species: parasites of
sympatric native and introduced snails. Oikos (in press).
Torchin, M. E., Lafferty, K. D. & Kuris, A. M. Release from parasites as natural enemies:
increased performance of a globally introduced marine crab. Biological Invasions (2002a).
Torchin, M. E., Lafferty, K. D. & Kuris, A. M. Parasites and marine invasions. Parasitology
(2002b).
128.
129.
130.
131.
132.
133.
134.
135.
136.
Torres, P. et al. Ecological aspects of nematode parasites of introduced salmonids from
Valdivia river basin, Chile. Memorias do Instituto Oswaldo Cruz Rio de Janeiro 86, 115-122
(1991).
Vincent, A. L. Parasites of the starling, Sturnus vulgaris, in San Diego County, California.
Journal of Parasitology 58 (1972).
Wallet, M., Theron, A. & Lambert, A. Shedding pattern of cercariae of Bucephalus
polymorphus (Trematoda, Bucephalidae) and its relationship to the activity of its host
Dreissena polymorpha (Lamellibranchia, Dreissenidae). Annales de Parasitologie Humaine et
Comparee 60, 675-684 (1985).
Weekes, P. J. & Penlington, B. First records of Ligula intestinalis (Cestoda) in rainbow trout,
Salmo gairdneri, and common bully, Gobiomorphus cotidianus, New Zealand. Journal of Fish
Biology 28, 183-190 (1986).
Whitlatch, R. B. Studies on the population ecology of the salt marsh gastropod Batillaria
zonalis. The Veliger 17, 47-55 (1974).
Williams, I. C. & Ellis, C. Movements of the common periwinkle, Littorina littorea (L.), on the
Yorkshire coast in winter and the influence of infection with larval digenea. Journal of
Experimental Marine Biology and Ecology 17, 47-58 (1975).
Winemiller, K. O. & Winsborough, B. M. Occurrence of Epizoic Communities on the Parasitic
Copepod Lernaea carassii (Lernaeidae). Southwestern Naturalist 35, 206-210 (1990).
Winterbourn, M. J. Larval Trematoda parasitizing the New Zealand species of Potamopyrgus
(Gastropoda: Hydrobiidae). Mauri Ora 2, 17-30 (1973).
Yamaguchi, T., Tokunaga, S. & Aratake, H. Contagious infection by the rhizocephalan parasite
Sacculina sp. in the grapsid crab Hemigrapsus sanguineus (De Haan). Crustacean Research 23,
89-101 (1994).