Supplementary Web Information (Torchin et al.) Examples of parasites and introduced species



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    1. Supplementary Web Information (Torchin et al.)

  1. 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.


  2. 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.

  1. Host Taxon

  1. Host Species

  1. References

Molluscs



Batillaria cumingii



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


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:
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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).

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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).

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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).

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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).

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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).

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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).

28. 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).

29. Conti, J. A. Helminths of Foxes and Coyotes Canis-latrans in Florida Usa. Proceedings of the Helminthological Society of Washington 51, 365-367 (1984).

30. 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).

31. 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).

32. 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).

33. Cooper, C. L. & Crites, J. L. Community ecology of helminth parasitism in an insular passerine avifauna. Journal of Parasitology 62, 105-110 (1976).

34. 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).

35. Curtis, L. A. Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries. Journal of Parasitology 83, 793-803 (1997).

36. 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).

37. 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 Fox-Chasing Enclosures. Journal of Wildlife Diseases 28, 581-589 (1992).

38. 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).

39. 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).

40. 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).

41. Dick, T. A. The atrium of the fish heart as a site for Contracaecum spp. larvae. Journal of Wildlife Diseases 23, 328-330 (1987).

42. 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).

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44. Dove, A. D. M. Richness patterns in the parasite communities of exotic poeciliid fishes. Parasitology 120, 609-623 (2000).

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47. 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).

48. 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).

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50. 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).

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54. 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).

55. 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).

56. 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).

57. 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).

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