Is there such thing as a parasite free lunch? the direct and indirect consequences of eating invasive prey

EcoHealth

Volumn 9, Issue 1, 2012, Pages 6-16

  Bulté, Grégory ^a   Robinson, Stacey A ^a   Forbes, Mark R ^a   Marcogliese, David J ^b  

^a CARLETON UNIVERSITY   (Canada)

^b ENVIRONMENT CANADA   (Canada)

Author keywords

contaminants; ecoimmunology; ecotoxicology; parasitology; predator prey relationships; trophic transfer

Indexed keywords

ANIMAL; ECOSYSTEM; FEEDING BEHAVIOR; FOOD CONTROL; HOST PARASITE INTERACTION; INTRODUCED SPECIES; PHYSIOLOGY; PREDATION; REVIEW; RISK FACTOR;

ANIMALS; ECOSYSTEM; FEEDING BEHAVIOR; FOOD PARASITOLOGY; HOST-PARASITE INTERACTIONS; INTRODUCED SPECIES; PREDATORY BEHAVIOR; RISK FACTORS;

EID: 84863217328     PISSN: 16129202     EISSN: 16129210     Source Type: Journal    
DOI: 10.1007/s10393-012-0757-7     Document Type: Review

References (87)

1. Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Canadian Journal of Zoology 79:101-105 (Pubitemid 32180250)
2. Andraso GM (2005) Summer food habits of pumpkinseeds (Lepomis gibbosus) and bluegills (Lepomis macrochirus) in Presque Isle Bay, Lake Erie. Journal of Great Lakes Research 31:397-404 (Pubitemid 43048754)
3. Bartsch MR, Bartsch LA, Gutreuter S (2005) Strong effects of predation by fishes on an invasive macroinvertebrate in a large floodplain river. Journal of the North American Benthological Society 24:169-177 (Pubitemid 40290145)
4. Beldomenico PM, Begon M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25:21-27
5. Bertrand MD, Marcogliese DJ, Magnan P (2008) Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. Journal of Fish Biology 72:555-572 (Pubitemid 351225066)
6. Boles LC, Lipcius RN (1997) Potential for population regulation of the zebra mussel by finfish and the blue crab in North American estuaries. Journal of Shellfish Research 16:179-186 (Pubitemid 27358174)
7. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD et al. (2003) The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161:1-28 (Pubitemid 36144810)
8. Bordes F, Morand S (2009) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118:801-806
9. Boughton RK, Joop G, Armitage SAO (2011) Outdoor immunology: methodological considerations for ecologists. Functional Ecology 25:81-100
10. Bulté G, Blouin-Demers G (2008) Northern map turtles (Graptemys geographica) derive energy from the pelagic pathway through predation on zebra mussels (Dreissena polymorpha). Freshwater Biology 53:497-508 (Pubitemid 351171224)
11. Bur MT, Stapanian MA, Bernhardt G, Turner MW (2008) Fall diets of red-breasted merganser (Mergus serrator) and walleye (Sander vitreus) in Sandusky Bay and adjacent waters of western Lake Erie. American Midland Naturalist 159:147-161 (Pubitemid 351280616)
12. Butler JRA, du Toit JT, Bingham J (2004) Free-ranging domestic dogs (Canis familiaris) as predators and prey in rural Zimbabwe: threats of competition and disease to large wild carnivores. Biological Conservation 115:369-378 (Pubitemid 37358489)
13. Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey - an acquired taste? Frontiers in Ecology and the Environment 7:525-532
14. Couillard CM, Macdonald RW, Courtnay SC, Palace VP (2008) Chemical- environment interactions affecting the risk of impacts on aquatic organisms: a review with a Canadian perspective - interactions affecting exposure. Environmental Reviews 16:1-17
15. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443-449
16. Dechtiar AO, Christie WJ (1988) Survey of the parasite fauna of Lake Ontario fishes, 1961 to 1971. In: Parasites of Fishes in the Canadian Waters of the Great Lakes, Nepszy SJ (editor), Ann Arbor, MI: Great Lakes Fishery Commission, 51: 66-95
17. Dechtiar AO, Lawrie AH (1988) Survey of the parasite fauna of Lake Superior fishes, 1969 to 1975. In: Parasites of Fishes in the Canadian Waters of the Great Lakes, Nepszy SJ (editor), Ann Arbor, MI: Great Lakes Fishery Commission, Technical Report No. 51: 1-18
18. Dechtiar AO and Nepszy SJ (1988) Survey of the parasite fauna of selected fish species from Lake Erie, 1970-1975. In: Parasites of Fishes in the Canadian Waters of the Great Lakes, Nepszy SJ (editor), Ann Arbor, MI: Great Lakes Fishery Commission, Technical Report No. 51: 49-65
19. Dechtiar AO, Collins JJ, Reckahn JA (1988) Survey of the parasite fauna of Lake Huron fishes, 1961 to 1971. In: Parasites of Fishes in the Canadian Waters of the Great Lakes, Nepszy SJ (editor), Ann Arbor, MI: Great Lakes Fishery Commission, Technical Report No. 51: 19-48
20. Dietrich JP, Morrison JP, Hoyle JA (2006) Alternative ecological pathways in the Eastern Lake Ontario food web - Round goby in the diet of lake trout. Journal of Great Lakes Research 32:395-400 (Pubitemid 44087172)
21. Dunn AM (2009) Parasites and biological invasions. Advances in Parasitology 68:161-184
22. Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058-1060
23. Estes JA (1996) Predators and ecosystems management. Wildlife Society Bulletin 24:390-396
24. Evans DM (1973) Seasonal variations in body composition and nutrition of the vole Microtus agrestis. Journal of Animal Ecology 42:1-18
25. Fairbrother A, Smits J, Grasman KA (2004) Avian immunotoxicology. Journal of Toxicology and Environmental Health Part B 7:105-137 (Pubitemid 38316641)
26. Fernie KJ, King RB, Drouillard KG, Stanford KM (2008) Temporal and spatial patterns of contaminants in Lake Erie watersnakes (Nerodia sipedon insularum) before and after the round goby (Apollonia melanostomus) invasion. Science of the Total Environment 406:344-351
27. Fitzsimons JD, Clark M, Keir M (2009) Addition of round gobies to the prey community of Lake Ontario and potential implications to thiamine status and reproductive success of Lake Trout. Aquatic Ecosystem Health & Management 12:296-312
28. French JRP, Bur MT (1996) The effect of zebra mussel consumption on growth in freshwater drum in Lake Erie. Journal of Freshwater Ecology 11:283-289. (Pubitemid 27012771)
29. Gendron AD, Marcogliese DJ, Barbeau S, Christin MS, Brousseau P, Ruby S, et al. (2003) Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469-476 (Pubitemid 36639466)
30. Gendron AD, Marcogliese DJ, Thomas M (2012) Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biological Invasions 14:367-384
31. Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Functional Ecology 25:5-17
32. Grasman KA, Fox GA, Scanlon PF, Ludwig JP (1996) Organochlorine- associated immunosuppression in prefledgling Caspian terns and herring gulls from the Great Lakes: an ecoepidemiological study. Environmental Health Perspectives 104:829-842 (Pubitemid 26290307)
33. Grimble RF (2001) Symposium on 'evidence-based nutrition' - Nutritional modulation of immune function. Proceedings of the Nutrition Society 60:389-397 (Pubitemid 32772455)
34. Herod JJ, Frey TL, Sickel JB (1997) Blue catfish (Ictalurus furcatus: Ictaluridae) predation on the zebra mussel in the Ohio River near Paducah, Kentucky. Transactions of the Kentucky Academy of Science 58:96
35. Jacobs GR, Madenjian CP, Bunnell DB, Holuszko JD (2010) Diet of lake trout and burbot in Northern Lake Michigan during spring: evidence of ecological interactions. Journal of Great Lakes Research 36:312-317
36. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61-67
37. Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske, SA, Poulin R, Thieltges DW (2010), When parasites become prey :ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25: 362-371
38. Johnson JH, Ross RM, McCullough RD, Mathers A (2010) Diet shift of double-crested cormorants in eastern Ontario associated with the expansion of the invasive round goby. Journal of Great Lakes Research 36:242-247
39. Jones LA, Houdijk JGM, Sakkas P, Bruce AD, Mitchell M, Knox DP et al. (2011) Dissecting the impact of protein versus energy host nutrition on the expression of immunity to gastrointestinal parasites during lactation. International Journal for Parasitology 41:711-719
40. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009a) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047-2056
41. Kelly DW, Paterson RA, Townsend C.R, Poulin R, Tompkins DM (2009b) Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 54:1805-1818
42. Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG et al. (2007) Effects of methylmercury exposure on the immune function of juvenile common loons (Gavia immer). Environmental Toxicology and Chemistry 26:1460-1469 (Pubitemid 47067328)
43. Kidd MT (2004) Nutritional modulation of immune function in broilers. Poultry Science 83:650-657 (Pubitemid 39197232)
44. King RM, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Canadian Journal of Zoology 84:108-115
45. Krist AC, Jokela J, Wiehn J, Lively CM (2004) Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction. Journal of Evolutionary Biology 17:33-40 (Pubitemid 38162177)
46. Kuris AM (2003) Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89:S96-S100
47. Kvach Y, Stepien CA (2008) Metazoan parasites of the introduced round and tubenose gobies in the Great Lakes: support for the "enemy release hypothesis". Journal of Great Lakes Research 34:23-35 (Pubitemid 351555516)
48. Kwon TD, Fisher SW, Kim GW, Hwang H, Kim JE (2006) Trophic transfer and biotransformation of polychlorinated biphenyls in zebra mussel, round goby, and smallmouth bass in Lake Erie, USA. Environmental Toxicology and Chemistry 25:1068-1078 (Pubitemid 46100052)
49. Lafferty KD (1999) The evolution of trophic transmission. Parasitology Today 15:111-115 (Pubitemid 29341191)
50. Lindeman PV (2006) Zebra and quagga mussels (Dreissena spp.) and other prey of a Lake Erie population of common map turtles (Emydidae: Graptemys geographica). Copeia 2006:268-273 (Pubitemid 43837102)
51. Madenjian CP, Stapanian MA, Witzel LD, Einhouse DW, Pothoven SA, Whitford HL (2011) Evidence for predatory control of the invasive round goby. Biological Invasions 13:987-1002
52. Magoulick DD, Lewis LC (2002) Predation on exotic zebra mussels by native fishes: effects on predators and prey. Freshwater Biology 47:1908-1918 (Pubitemid 35181212)
53. Marcogliese DJ, Dautremepuits C, Gendron AD, Fournier M (2010) Interactions between parasites and pollutants in yellow perch (Perca flavescens) in the St. Lawrence River, Canada: implications for resistance and tolerance to parasites. Canadian Journal of Zoology 88: 247-258
54. Marcogliese DJ, Pietrock M (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27: 123-130
55. Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195:129-148
56. Mastitsky SE, Veres JK (2010) Field evidence for a parasite spillback caused by exotic mollusc Dreissena polymorpha in an invaded lake. Parasitology Research 106:667-675
57. Mazak EJ, MacIsaac HJ, Servos MR, Hesslein R (1997) Influence of feeding habits on organochlorine contaminant accumulation in waterfowl on the Great Lakes. Ecological Applications 7:1133-1143 (Pubitemid 127447722)
58. Mercer JL, Fox MG, Metcalfe CD (1999) Changes in benthos and three littoral zone fishes in a shallow, eutrophic Ontario lake following the invasion of the zebra mussel (Dreissena polymorpha). Lake and Reservoir Management 15:310-323
59. Morrison TW, Lynch WE, Dabrowski K (1997) Predation on zebra mussels by freshwater drum and yellow perch in Western Lake Erie. Journal of Great Lakes Research 23:177-189 (Pubitemid 27347428)
60. Muzzall PM (1999) Nematode parasites of yellow perch, Perca flavescens, from the Laurentian Great Lakes. Journal of the Helminthological Society of Washington 66: 115-122 (Pubitemid 29380839)
61. Muzzall PM, Whelan G (2011) Parasites of fish from the Great Lakes: a synopsis and review of the literature, 1871-2010. Great Lakes Fishery Commission, Ann Arbor, MI
62. Ostfeld RS, Holt RD (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic diseases reservoirs. Frontiers in Ecology and the Environment 2:13-20
63. Patterson JC, Lindeman PV (2009) Effects of zebra and quagga mussel (Dreissena spp.) invasion on the feeding habits of Sternotherus odoratus (stinkpot) on Presque Isle, northwestern Pennsylvania. Northeastern Naturalist 16:365-374
64. Perkins SE, Altizer S, Bjornstad O, Burdon JJ, Clay K, Gómez-Aparicio L, Jeschke JM, Johnson PTJ, Lafferty KD, Malmstrom CM, Martin P, Power A, Strayer DL, Thrall PH, Uriarte M (2008) Invasion biology and parasitic infections. In: Infectious Disease Ecology, Ostfeld RS, Keesing F, Eviner VT (editors), Princeton: Princeton University Press, pp. 179-204
65. Petrie SA, Knapton RW (1999) Rapid increase and subsequent decline of zebra and quagga mussels in Long Point Bay, Lake Erie: possible influence of waterfowl predation. Journal of Great Lakes Research 25:772-782 (Pubitemid 30166002)
66. Pothoven SA, Nalepa TF, Schneeberger PJ, Brandt SB (2001) Changes in diet and body condition of lake whitefish in southern Lake Michigan associated with changes in benthos. North American Journal of Fisheries Management 21:876-883 (Pubitemid 33065983)
67. Reyjol Y, Brodeur P, Mailhot Y, Mingelbier M, Dumont P (2010) Do native predators feed on non-native prey? The case of the round goby in a fluvial piscivorous fish assemblage. Journal of Great Lakes Research 36:618-624
68. Richman SE, Lovvorn JR (2004) Relative foraging value to lesser scaup ducks of native and exotic clams from San Francisco Bay. Ecological Applications 14:1217-1231 (Pubitemid 39188069)
69. Ripple WJ, Beschta RL (2005) Linking wolves and plants: Aldo Leopold on trophic cascades. Bioscience 55:613-621 (Pubitemid 40912687)
70. Rossiter W, Sukhdeo MVK (2011) Exploitation of asymmetric predator-prey interactions by trophically transmitted parasites. Oikos 120:607-614
71. Ruetz CR, Strouse DL, Pothoven SA (2009) Energy density of introduced round goby compared with four native fishes in a Lake Michigan tributary. Transactions of the American Fisheries Society 138:938-947
72. H Schulenburg J Kurtz Y Moret MT Siva-Jothy 2009 Introduction. Ecological immunology Philosophical Transactions of the Royal Society: Biological Sciences 364 3 14 10.1098/rstb.2008.0249 10.1098/rstb.2008.0249 Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (2009) Introduction. Ecological immunology. Philosophical Transactions of the Royal Society: Biological Sciences 364:3-14.doi: 10.1098/rstb.2008.0249
73. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11:317-321 (Pubitemid 126382139)
74. Sietman BE, Dunn HL, Tucker JK, Kelner DE (2003) Muskrat (Ondatra zibethicus) predation on zebra mussels (Dreissena polymorpha) attached to unionid bivalves. Journal of Freshwater Ecology 18:25-32 (Pubitemid 36439827)
75. Somers CM, Lozer MN, Kjoss VA, Quinn JS (2003) The invasive round goby (Neogobius melanostomus) in the diet of nestling double-crested cormorants (Phalacrocorax auritus) in Hamilton Harbour, Lake Ontario. Journal of Great Lakes Research 29:392-399 (Pubitemid 37269136)
76. Southward Hogan L, Marschall E, Folt C, Stein RA (2007) How non-native species in Lake Erie influence trophic transfer of mercury and lead to top predators. Journal of Great Lakes Research 33:46-61 (Pubitemid 46624385)
77. Steinhart GB, Stein RA, Marschall EA (2004) High growth rate of young-of-the-year smallmouth bass in Lake Erie: a result of the round goby invasion? Journal of Great Lakes Research 30:381-389 (Pubitemid 39385246)
78. Suarez AV, Richmond JQ, Case TJ (2000) Prey selection in horned lizards following the invasion of Argentine ants in southern California. Ecological Applications 10:711-725 (Pubitemid 32139518)
79. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:S137-S151
80. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628-630 (Pubitemid 36227669)
81. Truemper HA, Lauer TE (2005) Gape limitation and piscine prey size-selection by yellow perch in the extreme southern area of Lake Michigan, with emphasis on two exotic prey items. Journal of Fish Biology 66:135:149
82. Tucker JK, Cronin, FA, Soergel DW, Theiling CH (1996) Predation on zebra mussels (Dreissena polymorpha) by common carp (Cyprinus carpio). Journal of Freshwater Ecology 11:363-372 (Pubitemid 27012778)
83. Valtonen ET, Marcogliese DJ, Julkunen M (2010) Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162:139-152
84. Watzin MC, Joppe-Mercure K, Rowder J, Lancaster B, Bronson L (2008) Significant fish predation on zebra mussels Dreissena polymorpha in Lake Champlain, U.S.A. Journal of Fish Biology 73: 1585-1599
85. Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M (2003a) Parasite selection for immunogenetic optimality. Science 301:1343 (Pubitemid 37075801)
86. Wegner KM, Reusch TBH, Kalbe M (2003b) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. Journal of Evolutionary Biology 16:224-232 (Pubitemid 36261053)
87. Wormington A, Leach JH (1992) Concentrations of migrant diving ducks at Point Pelee National Park, Ontario, in response to invasion of zebra mussels, Dreissena polymorpha. Canadian Field Naturalist 106:376-380 (Pubitemid 24412985)