Some (worms) like it hot: Fish parasites grow faster in warmer water, and alter host thermal preferences

Global Change Biology

Volumn 18, Issue 5, 2012, Pages 1540-1548

  Macnab, Vicki ^a   Barber, Iain ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Behavioural manipulation; Global climate change; Host parasite interactions; Schistocephalus solidus; Sticklebacks; Temperature

Indexed keywords

CLIMATE CHANGE; ECOSYSTEM HEALTH; FECUNDITY; FLATWORM; GLOBAL CLIMATE; GROWTH RATE; HOST PREFERENCE; HOST-PARASITE INTERACTION; MICROHABITAT; PARASITE PREVALENCE; PARASITE TRANSMISSION; TELEOST; TEMPERATURE EFFECT;

AVES; CESTODA; GASTEROSTEUS ACULEATUS; SCHISTOCEPHALUS SOLIDUS;

EID: 84859486148     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2011.02595.x     Document Type: Article

References (80)

1. Adams CE, Brown DW, Keay L (1994) Elevated predation risk associated with inshore migrations of fish in a large lake, Loch Lomond, Scotland. Hydrobiologia, 290, 135-138.
2. Allen JRM, Wootton RJ (1982) The effect of ration and temperature on the growth of the 3-spined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology, 20, 409-422.
3. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution, 19, 535-544.
4. Arme C (1968) Effects of the plerocercoid larva of a pseudophyllidean cestode, Ligula intestinalis, on the pituitary gland and gonads of its host. Biological Bulletin, Marine Biological Laboratory, Woods Hole, 134, 15-25.
5. Arme C, Owen RW (1967) Infections of the three spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology, 57, 301-314.
6. Barber I (1997) A non-invasive morphometric technique for estimating cestode plerocercoid burden in small freshwater fish. Journal of Fish Biology, 51, 654-658.
7. Barber I, Arnott SA (2000) Split-clutch IVF: a technique to examine indirect fitness consequences of mate preferences in sticklebacks. Behaviour, 137, 1129-1140.
8. Barber I, Scharsack JP (2010) The three-spined stickleback - Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology, 137, 411-424.
9. Barber I, Svensson PA (2003) Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology, 126, 359-367.
10. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries, 10, 131-165.
11. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proceedings of the Royal Society of London, Series B: Biological Sciences, 268, 71-76.
12. Barber I, Walker P, Svensson PA (2004) Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour, 141, 1425-1440.
13. Barber I, Wright H, Arnott S, Wootton R (2008) Growth and energetics in the stickleback-Schistocephalus host-parasite system: a review of experimental infection studies. Behaviour, 145, 647-668.
14. Bates AE, Leiterer F, Wiedeback ML, Poulin R (2011) Parasitized snails take the heat: a case of host manipulation? Oecologia, 167, 613-621.
15. Blanar CA, Munkittrick KR, Houlahan J, Maclatchy DL, Marcogliese DJ (2009) Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquatic Toxicology, 93, 18-28.
16. Bonga SEW (1997) The stress response in fish. Physiological Reviews, 77, 591-625.
17. Chellappa S, Huntingford FA, Strang RHC, Thomson RY (1995) Condition factor and hepatosomatic index as estimates of energy status in male 3-spined stickleback. Journal of Fish Biology, 47, 775-787.
18. Clarke AS (1954) Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus. Proceedings of the Zoological Society of London, 124, 257-302.
19. Cowx IG, Rollins D, Tumwebaze R (2008) Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. Journal of Fish Biology, 73, 2249-2260.
20. 2 and climate change: results from six dynamic global vegetation models. Global Change Biology, 7, 357-373.
21. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica, 78, 103-116.
22. Davies PS, Walkey M (1966) The effect of body size and temperature upon oxygen consumption of the cestode Schistocephalus solidus (Müller). Comparative Biochemistry and Physiology, 18, 415-425.
23. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences, USA, 105, 6668-6672.
24. Dobson AP (2009) Climate variability, global change, immunity, and the dynamics of infectious diseases. Ecology, 90, 920-927.
25. Dörücü M, Wilson D, Barber I (2007) Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks. Journal of Parasitology, 93, 1521-1523.
26. EEA (2010) The European Environment - State and Outlook 2010: Synthesis. European Environment Agency, Copenhagen, Denmark.
27. Elliot SL, Blanford S, Thomas MB (2002) Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proceedings of the Royal Society of London, Series B: Biological Sciences, 269, 1599-1607.
28. Eure H (1976) Seasonal abundance of Neoechinorhynchus cylindratus taken from largemouth bass (Micropterus salmoides) in a heated reservoir. Parasitology, 73, 355-370.
29. Fialho RF, Schall JJ (1995) Thermal ecology of a malarial parasite and its insect vector: consequences for the parasites transmission success. Journal of Animal Ecology, 64, 553-562.
30. Garside ET, Heinze DG, Barbour SE (1977) Thermal preference in relation to salinity in threespine stickleback, Gasterosteus aculeatus L., with an interpretation of its significance. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 55, 590-594.
31. Guderley H, Leroy PH (2001) Family origin and the response of threespine stickleback, Gasterosteus aculeatus, to thermal acclimation. Journal of Comparative Physiology, B, 171, 91-101.
32. Hammerschmidt K, Kurtz J (2005) Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proceedings of the Royal Society B-Biological Sciences, 272, 2511-2518.
33. Hammerschmidt K, Koch K, Milinski M, Chubb JC, Parker GA (2009) When to go: optimization of host switching in parasites with complex life cycles. Evolution, 63, 1976-1986.
34. Harvell CD, Kim K, Burkholder JM et al. (1999) Review: marine ecology - emerging marine diseases - climate links and anthropogenic factors. Science, 285, 1505-1510.
35. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Ecology - climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.
36. Heins DC, Baker JA (2008) The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour, 145, 625-645.
37. Herrmann KK, Poulin R (2011) Life cycle truncation in a trematode: does higher temperature indicate shorter host longevity? International Journal for Parasitology, 41, 697-704.
38. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
39. Höglund J, Thulin J (1990) The epidemiology of the metacercariae of Diplostomum baeri and Diplostomum spathaceum in perch (Perca fluviatilis) from the warm water effluent of a nuclear-power station. Journal of Helminthology, 64, 139-150.
40. I.P.C.C. (2007) Summary for policymakers. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climage Change. (ed. Solomon SQD, Manning M, Chen Z, Manning M, Averyt KB, Tignor M, Miller HL), pp. 1-18. Cambridge University Press, Cambridge and New York.
41. Johnson PTJ, Townsend AR, Cleveland CC et al. (2010) Linking environmental nutrient enrichment and disease emergence in humans and wildlife. Ecological Applications, 20, 16-29.
42. Jordan CM, Garside ET (1972) Upper lethal temperatures of threespine stickleback, Gasterosteus aculeatus (L), in relation to thermal and osmotic aclimation, ambient salinity, and size. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 50, 1405.
43. Kollner B, Kotterba G (2002) Temperature dependent activation of leucocyte populations of rainbow trout, Oncorhynchus mykiss, after intraperitoneal immunisation with Aeromonas salmonicida. Fish & Shellfish Immunology, 12, 35-48.
44. Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology, 90, 888-900.
45. Lester RJG (1971) Influence of Schistocephalus plerocercoids on respiration of Gasterosteus and a possible resulting effect on behavior of fish. Canadian Journal of Zoology, 49, 361-366.
46. Lv S, Zhou XN, Zhang Y et al. (2006) The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitology Research, 99, 583-587.
47. Macnab VL, Katsiadaki I, Barber I (2009) Reproductive potential of Schistocephalus solidus infected male three-spined stickleback Gasterosteus aculeatus from two UK populations. Journal of Fish Biology, 75, 2095-2107.
48. Macnab V, Scott AP, Katsiadaki I, Barber I (2011) Variation in the reproductive potential of Schistocephalus infected male sticklebacks is associated with 11-ketotestosterone titre. Hormones and Behavior, 60, 371-379.
49. Marcogliese DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Revue Scientifique Et Technique De L'Office International Des Epizooties, 27, 467-484.
50. Marshall J, Cowx IG (2003) Will the explosion of Ligula Intestinalis in Rastrineobola argentea lead to another shift in the fisheries of Lake Victoria? In: Interactions between Fish and Birds: Implications for Management. (ed. Cowx IG), pp. 244-256. Blackwell Science, Oxford, UK.
51. McMichael AJ, Campbell-Lendrum DH, Corvalán CF, Ebi KL, Githeko AK, Scheraga JD, Woodward A (2003) Climate Change and Human Health. Risks and Responses. World Health Organization, Geneva, Switzerland.
52. McMichael AJ, Woodruff RE, Hales S (2006) Climate change and human health: present and future risks. Lancet, 367, 859-869.
53. Meakins RH, Walkey M (1975) Effects of parasitism by plerocercoid of Schistocephalus solidus Müller 1776 (Pseudophyllidea) on respiration of 3-spined stickleback Gasterosteus aculeatus L. Journal of Fish Biology, 7, 817-824.
54. Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour, 93, 203-215.
55. Müller CB, Schmid-Hempel P (1993) Exploitation of cold temperature as defense against parasitoids in bumblebees. Nature, 363, 65-67.
56. Nikoskelainen S, Bylund G, Lilius EM (2004) Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Developmental & Comparative Immunology, 28, 581-592.
57. Parker GA, Chubb JC, Ball MA, Roberts GN (2003) Evolution of complex life cycles in helminth parasites. Nature, 425, 480-484.
58. Pascoe D, Mattey D (1977) Dietary stress in parasitized and non-parasitized Gasterosteus aculeatus L. Zeitschrift Fur Parasitenkunde-Parasitology Research, 51, 179-186.
59. Pascual M, Dobson AP, Bouma MJ (2009) Underestimating malaria risk under variable temperatures. Proceedings of the National Academy of Sciences of the United States of America, 106, 13645-13646.
60. Patz JA, Epstein PR, Burke TA, Balbus JM (1996) Global climate change and emerging infectious diseases. Jama-Journal of the American Medical Association, 275, 217-223.
61. Patz JA, Githeko AK, Mccarty JP, Hussein S, Confalonieri U, De Wet N (2003) Climate change and infectious diseases. In: Climate Change and Human Health. Risks and Responses. (eds Mcmichael AJ, Campbell-Lendrum DH, Corvalán CF, Ebi KL, Githeko AK, Scheraga JD, Woodward A) pp. 103-132. World Health Organization, Geneva, Switzerland.
62. Pounds JA, Bustamante MR, Coloma LA et al. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439, 161-167.
63. Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PPC, Baylis M (2005) Climate change and the recent emergence of bluetongue in Europe. Nature Reviews: Microbiology, 3, 171-181.
64. Reimchen TE (1994) Predators and morphological evolution in threespine stickleback. In: Evolutionary Biology of the Threespine Stickleback (eds Bell MA, Foster SA) pp. 240-276. Oxford University Press, Oxford, UK.
65. Reynolds WW, Casterlin ME, Covert JB (1976) Behavioral fever in teleost fishes. Nature, 259, 41-42.
66. Rushbrook BJ, Katsiadaki I, Barber I (2007) Spiggin levels are reduced in male sticklebacks infected with Schistocephalus solidus. Journal of Fish Biology, 71, 298-303.
67. Scharsack JP, Koch K, Hammerschmidt K (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society of London, Series B: Biological Sciences, 274, 3151-3158.
68. Seppänen E, Kuukka H, Voutilainen A, Huuskonen H, Peuhkuri N (2009) Metabolic depression and spleen and liver enlargement in juvenile Arctic charr Salvelinus alpinus exposed to chronic parasite infection. Journal of Fish Biology, 74, 553-561.
69. Smyth JD (1946) Studies on tapeworm physiology. I. The cultivation of Schistocephalus solidus in vitro. Journal of Experimental Biology, 23, 47-70.
70. Smyth JD (1969) The Physiology of Cestodes. Oliver & Boyd, Edinburgh, UK.
71. Smyth JD (1994) Introduction to Animal Parasitology. Cambridge University Press, Cambridge, UK.
72. Studer A, Thieltges DW, Poulin R (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology-Progress Series, 415, 11-22.
73. Thomas MB, Blanford S (2003) Thermal biology in insect-parasite interactions. Trends in Ecology & Evolution, 18, 344-350.
74. Tierney JF, Crompton DWT (1992) Infectivity of plerocercoids of Schistocephalus solidus (Cestoda, Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. Journal of Parasitology, 78, 1049-1054.
75. Tierney JF, Huntingford FA, Crompton DWT (1993) The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behavior of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour, 46, 603-605.
76. Tierney JF, Huntingford FA, Crompton DWT (1996) Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology, 49, 483-493.
77. Vaughn LK, Bernheim HA, Kluger MJ (1974) Fever in lizard Dipsosaurus dorsalis. Nature, 252, 473-474.
78. Wedekind C (1997) The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitology, 115, 317-324.
79. Wedekind C, Strahm D, Scharer L (1998) Evidence for strategic egg production in a hermaphroditic cestode. Parasitology, 117, 373-382.
80. Weyts FAA, Cohen N, Flik G, Verburg-Van Kemenade BML (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish & Shellfish Immunology, 9, 1-20.