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. 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).
2. Sakanari, J. A. & Moser, M. Adaptation of an introduced host to an indigenous parasite. Journal of Parasitology 76, 420-423 (1990).
3. Blaustein, A. R., Kuris, A. M. & Alió, J. J. Pest and parasite species-richness problems. American Naturalist 122, 556-566 (1983).
4. Cornell, H. V. & Hawkins, B. A. in Parasitoid Community Ecology (eds. Hawkins, B. A. & Sheehan, W.) 77-89 (Oxford University Press, Oxford, 1994).
5. 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).
6. Combes, C. Parasitism: the ecology and evolution of intimate interactions (ed. Thompson, J. N.) (University of Chicago Press, Chicago, 2001).
7. CIESM. Atlas of exotic species in the Mediterranean Sea http://www.ciesm.org/atlas/index/html., (2001).
8. 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).
9. 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).
10. USGS. US Geological Survey Nonindigenous Aquatic Species http://nas.er.usgs.gov., (2001).
11. 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
/Host Species
/References
Molluscs / Batillaria cumingii / Harada and Suguri, 1989; Rybakov and Lukomskaya, 1986; Shimura andIto, 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 / 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
Mammals / Rattus rattus / 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
Mammals / Trichosurus vulpecula / O'Callaghan and Moore, 1986; Presidente et al., 1982; *Stankiewicz
et al., 1998
Mammals / Vulpes vulpes / 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. 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).
2. 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).
3. Barton, D. P. & Pichelin, S. Acanthocephalus bufonis (Acanthocephala) from Bufo marinus (Bufonidae: Amphibia) in Hawaii. Parasite 6, 269-272 (1999).
4. Blasco, S. et al. The helminthfauna of Oryctolagus cuniculus (Linnaeus, 1758) in the Iberian Peninsula. Faunistic and ecological considerations. Parasite 3, 327-333 (1996).
5. Boag, B. The incidence of helminth parasites from the wild rabbit Oryctolagus cuniculus in Eastern Scotland [UK]. Journal of Helminthology 59, 61-69 (1985).
6. 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).
7. 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).
8. 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).
9. 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. 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).
11. 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).
12. Boyd, E. M. A survey of parasitism of the starling Sturnus vulgaris L. in North America. Journal of Parasitology 37, 56-84 (1951).
13. Brasil, M. D. C. & Amato, S. B. Faunistic Analysis of the Helminths of Sparrows Passer-domesticus L. 1758 Captured in Campo Grande Rio de Janeiro Rj. Memorias do Instituto Oswaldo Cruz Rio de Janeiro 87, 43-48 (1992).
14. 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, 2224-2229 (1985).
15. 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).
16. 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).
17. 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).
18. 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).
19. 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).
20. Butler, F. T. Arthropod and helminth parasites from rabbits Oryctolagus cuniculus in south-west Ireland. Irish Naturalists' Journal 24, 392-395 (1994).
21. 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).
22. 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).
23. 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).
24. 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).
25. 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).
26. Coman, B. J. Helminth parasites of the fox (Vulpes vulpes) in Victoria. Australian Veterinary Journal 49, 378-384 (1973).
27. 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).