Host-parasite interactions in food webs: Diversity, stability, and coevolution

Food Webs

Volumn 6, Issue , 2016, Pages 1-8

  Jephcott, Thomas G ^a   Sime Ngando, Telesphore ^b,c   Gleason, Frank H ^d   Macarthur, Deborah J ^e  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITÉ BLAISE PASCAL   (France)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d UNIVERSITY OF SYDNEY   (Australia)

^e AUSTRALIAN CATHOLIC UNIVERSITY   (Australia)

Author keywords

Ecological networks; Energy transfer; Food webs; Parasites

Indexed keywords

EID: 84952760331     PISSN: None     EISSN: 23522496     Source Type: Journal    
DOI: 10.1016/j.fooweb.2015.12.001     Document Type: Review

References (102)

1. Allesina S., Pascual M. Food web models: a plea for groups. Ecol. Lett. 2009, 12:652-662. 10.1111/j.1461-0248.2009.01321.x.
2. Allesina S., Tang S. Stability criteria for complex ecosystems. Nature 2012, 483:205-208. 10.1038/nature/10832.
3. Allesina S., Alonso D., Pascual M. A general model for food web structure. Science 2008, 320:658-661. 10.1126/science.1156269.
4. Amundsen P.A., Lafferty K.D., Knudsen R., Primicerio R., Klemesten A., Kuris A.M. Food web topology and parasites in the pelagic zone of a subartic lake. J. Anim. Ecol. 2009, 78:563-572. 10.1111/j.1365-2656.2008.01518.x.
5. Baiser B., Russell G.J., Lockwood J.L. Connectance determines invasion success via trophic interactions in model food webs. Oikos 2010, 119:1970-1976. 10.1111/j.1600-0706.2010.18557.x.
6. Barribeau S.M., Sadd B., du Plessis L., Schmid-Hempel P. Gene expression differences underlying genotype-by-genotype specificity in host-parasite system. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:3496-3501. 10.1073/pnas.1318628111.
7. Blaylock R.B., Bullard S.A. Counter-insurgents of the Blue Revolution? Parasites and diseases affecting aquaculture and science. J. Parasitol. 2014, 100:743-755. 10.1645/14-605.1.
8. Bondad-Reantaso M.G., Subasinghe R.P., Arthur J.R., Ogawa K., Chinabut S., Adlard R., Tan Z., Shariff M. Disease and health management in Asian aquaculture. Vet. Parasitol. 2005, 132:249-272. 10.1016/j.vetpar.2005.07.005.
9. Bukovinszky T., van Veen F.J.F., Jongema Y., Dicke M. Direct and indirect effects of resource quality on food web structure. Science 2008, 319:804-807. 10.1126/science.1148310.
10. Byers J.E. Including parasites in food webs. Trends Parasitol. 2009, 25:55-57. 10.1016/j.pt.2008.11.003.
11. Cirtwill A.R., Stouffer D.B. Concomitant predation on parasites is highly variable but constrains the way in which parasites contribute to food web structure. J. Anim. Ecol. 2015, 84:734-744. 10.1111/1365-2656.12323.
12. Cohen J.E., Newman C.M. A stochastic theory of community food webs I. Models and aggregated data. Proc. R. Soc. Lond. Biol. 1985, 224:421-448. 10.1098/rspb.1985.0042.
13. de Vries F.T., Liiri M.E., Bjørnlund L., Bowker M.A., Christensen S., Setälä H.M., Bardgett R.D. Land use alters the resistance and resilience of soil food webs to drought. Nat. Clim. Chang. 2012, 2:276-280. 10.1038/nclimate1368.
14. Demopoulos A.W.J., Sikkel P.C. Enhanced understanding of ectoparasite-host trophic linkages on coral reefs through stable isotope analysis. Int. J. Parasitol. Parasites Wildl. 2015, 4:125-134. 10.1016/j.ijppaw.2015.01.002.
15. Dercole F., Ferriere R., Rinaldi S. Chaotic Red Queen coevolution in three-species food chains. Proc. R. Soc. B 2010, 277:2321-2330. 10.1098/rspb.2010.0209.
16. Digel C., Curtsdotter A., Riede J., Klarner B., Brose U. Unravelling the complex structure of forest soil food webs: higher omnivory and more trophic levels. Oikos 2014, 123:1157-1172. 10.1111/oik.00865.
17. Dobson A., Allesina S., Lafferty K., Pascual M. The assembly, collapse, and restoration of food webs. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2009, 364:1803-1806. 10.1098/rstb.2009.0002.
18. Dunne J.A., Williams R.J., Martinez N.D. Food-web structure and network theory: the role of connectance and size. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12917-12922. 10.1073/pnas.192407699.
19. Dunne J.A., Williams R.J., Martinez N.D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 2002, 5:558-567. 10.1046/j.1461-0248.2002.00354.x.
20. Dunne J.A., Williams R.J., Martinez N.D. Network structure and robustness of marine food webs. Mar. Ecol. Prog. Ser. 2004, 273:291-302. 10.3354/meps273291.
21. Dunne J.A., Lafferty K.D., Dobson A.P., Hechinger R.F., Kuris A.M., Martinez N.D., McLaughlin J.P., Mouritsen K.N., Poulin R., Reise K., Stouffer D.B., Thieltges D.W., Williams R.J., Zander C.D. Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biol. 2013, 11. 10.1371/journal.pbio.1001579.
22. Ellner S.P., Becks L. Rapid prey evolution and the dynamics of two-predator food webs. Theor. Ecol. 2011, 4:133-152. 10.1007/s12080-010-0096-7.
23. Elton C. The Ecology Of Invasions By Animals And Plants 1958, University of Chicago Press, Chicago, (ISBN: 978-0-226-20638-7).
24. Fahimipour A.K., Hein A.M. The dynamics of assembling food webs. Ecol. Lett. 2014, 17:606-613. 10.1111/ele.12264.
25. Foley J.A., DeFries R., Asner G.P., Barford C., Bonan G., Carpenter S.R., Chapin F.S., Coe M.T., Daily G.C., Gibbs H.K., Helkowski J.H., Holloway T., Howard E.A., Kucharik C.J., Monfreda C., Patz J.A., Prentice I.C., Ramankutty N., Snyder P.K. Global consequences of land use. Science 2005, 309:570-574. 10.1126/science.1111772.
26. Gagic V., Hänke S., Thies C., Scherber C., Tomanović Z., Tscharntke T. Agricultural intensification and cereal aphid-parasitoid-hyperparasitoid food webs: network complexity, temporal variability and parasitism rates. Oecologia 2012, 170:1099-1109. 10.1007/s00442-012-2366-0.
27. Geyer J., Kiefer I., Kreft S., Chavez V., Salafsky N., Jeltsch F., Ibisch P.L. Classification of climate-change-induced stresses on biological diversity. Conserv. Biol. 2011, 25:708-715. 10.1111/j.1523-1739.2011.01676.x.
28. Gleason F.H., Kagami M., Lefèvre E., Sime-Ngando T. The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol. Rev. 2008, 22:17-25. 10.1016/j.fbr.2008.02.001.
29. Gleason F.H., Jephcott T.G., Küpper F.C., Gerphagnon M., Sime-Ngando T., Karpov S.A., Guillou L., van Ogtrop F.F. Potential roles for recently discovered chytrid parasites in the dynamics of harmful algal blooms. Fungal Biol. Rev. 2015, 29:20-33. 10.1016/j.fbr.2015.03.002.
30. Harvey J.A., Snaas H., Malcicka M., Visser B., Bezemer T.M. Small-scale spatial resource partitioning in a hyperparasitoid community. Arthropod Plant Interact. 2014, 8:393-401. 10.1007/s11829-014-9319-y.
31. Hechinger R.F. Parasites help find universal ecological rules. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:1656-1657. 10.1073/pnas.1423785112.
32. Hechinger R.F., Lafferty K.D., Dobson A.P., Brown J.H., Kuris A.M. A common scaling rule for abundance, energetics, and production of parasitic and free-living species. Science 2011, 333:445-447. 10.1126/science.1204337.
33. Hechinger R.F., Lafferty K.D., McLaughlin J.P., Fredensborg B.L., Huspeni T.C., Lorda J., Sandhu P.K., Shaw J.C., Torchin M.E., Whitney K.L., Kuris A.M. Food webs including parasites, biomass, body sizes, and life stages for three California/Baja California Estuaries. Ecology 2011, 92:791. 10.1890/10-1383.1.
34. Hechinger R.F., Wood A.C., Kuris A.M. Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proc. R. Soc. B 2011, 278:656-665. 10.1098/rspb.2010.1753.
35. Hernandez A.D., Sukhdeo M.V.K. Parasites alter the topology of a stream food web across seasons. Oecologia 2008, 156:613-624. 10.1007/s00442-008-0999-9.
36. Hudson P.J., Dobson A.P., Lafferty K.D. Is a healthy ecosystem one that is rich in parasites?. Trends Ecol. Evol. 2006, 21:381-385. 10.1016/j.tree.2006.04.007.
37. Huxham M., Raffaelli D., Pike A. Parasites and food web patterns. J. Anim. Ecol. 1995, 64:168-176. 10.2307/5752.
38. Janse J.H., Kuiper J.J., Weijters M.J., Westerbeek E.P., Jeuken M.H.J.L., Bakkenes M., Alkemade R., Mooij W.M., Verhoeven J.T.A. GLOBIO-Aquatic, a global model of human impact on the biodiversity of inland aquatic ecosystems. Environ. Sci. Pol. 2015, 48:99-114. 10.1016/j.envsci.2014.12.007.
39. Jephcott T.G., Alves-de-Souza C., Gleason F.H., van Ogtrop F., Sime-Ngando T., Karpov S., Guillou L. Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Fungal Ecol. 2016, 19:47-58. 10.1016/j.funeco.2015.03.007.
40. Johnson P.T.J., Buller I.D. Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. Ecology 2011, 92:535-541. 10.1890/10-0570.1.
41. Kim K.C., Byrne L.B. Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecol. Res. 2006, 21:794-810. 10.1007/s11284-006-0035-7.
42. Krofel M., Kos I., Jerina K. The noble cats and the big bad scavengers: effects of dominant scavengers on solitary predators. Behav. Ecol. Sociobiol. 2012, 66:1297-1304. 10.1007/s00265-012-1384-6.
43. Kuris A.M., Hechinger R.F., Shaw J.C., Whitney K.L., Aguirre-Macedo L., Boch C.A., Dobson A.P., Dunham E.J., Fredensborg B.L., Huspeni T.C., Lorda J., Mababa L., Mancini F.T., Mora A.B., Pickering M., Talhouk N.L., Torchin M.E., Lafferty K.D. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 2008, 454:515-518. 10.1038/nature06970.
44. Lafferty K.D. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol. Appl. 2004, 14:1566-1573. 10.1890/03-5088.
45. Lafferty K.D., Kuris A.M. Trophic strategies, animal diversity and body size. Trends Ecol. Evol. 2002, 17:507-513. 10.1016/S0169-5347(02)02615-0.
46. Lafferty K.D., Dobson A.P., Kuris A.M. Parasites dominate food web links. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:11211-11216. 10.1073/pnas.0604755103.
47. Lafferty K.D., Allesina S., Arim M., Briggs C.J., De Leo G., Dobson A.P., Dunne J.A., Johnson P.T.J., Kuris A.M., Marcogliese D.J., Martinez N.D., Memmott J., Marquet P.A., McLaughlin J.P., Mordecai E.A., Pascual M., Poulin R., Thieltges D.W. Parasites in food webs: the ultimate missing links. Ecol. Lett. 2008, 11:533-546. 10.1111/j.1461-0248.2008.01174.x.
48. Lapchin L. Host-parasitoid association and diffuse coevolution: when to be a generalist?. Am. Nat. 2002, 160:245-254. 10.1086/341020.
49. Lawton J.H., Warren P.H. Static and dynamic explanations for patterns in food webs. Trends Ecol. Evol. 1988, 3:242-245. 10.1016/0169-5347(88)90167-X.
50. Leander B.S., Hoppenrath M. Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). Eur. J. Protistol. 2008, 44:55-70. 10.1016/j.ejop.2007.08.004.
51. Lima dos Santos C.A.M., Howgate P. Fishborne zoonotic parasites and aquaculture: a review. Aquaculture 2011, 318:253-261. 10.1016/j.aquaculture.2011.05.046.
52. MacArthur R. Fluctuations of animal and populations and a measure of community stability. Ecology 1955, 36:533-536. 10.2307/1929601.
53. Marcogliese D.J., Cone D.K. Food webs: a plea for parasites. Trends Ecol. Evol. 1997, 12:320-325. 10.1016/S0169-5347(97)01080-X.
54. May R.M. Will a large complex system be stable?. Nature 1972, 238:413-414. 10.1038/238413a0.
55. Moloney C.L., St John M.A., Denman K.L., Karl D.M., Köster F.W., Sundby S., Wilson R.P. Weaving marine food webs from end to end under global change. J. Mar. Syst. 2011, 84:106-116. 10.1016/j.jmarsys.2010.06.012.
56. Mouillot D., Krasnov B.R., Poulin R. High intervality explained by phylogenetic constraints in host-parasite webs. Ecology 2008, 89:2043-2051. 10.1890/07-1241.1.
57. Mouritsen K.N., Poulin R., McLaughlin J.P., Thieltges D.W. Food web including metazoan parasites for an intertidal ecosystem in New Zealand: Ecological Archives E092-173. Ecology 2011, 92:2006. 10.1890/11-0371.1.
58. Murakami M., Hirao T., Kasei A. Effects of habitat configuration on host-parasitoid food web structure. Ecol. Res. 2008, 23:1039-1049. 10.1007/s11284-008-0478-0.
59. Nowak B.F. Parasitic diseases in marine cage culture - an example of experimental evolution of parasites?. Int. J. Parasitol. 2007, 37:581-588. 10.1016/j.ijpara.2007.01.003.
60. Ogawa K. Marine parasitology with special reference to Japanese fisheries and mariculture. Vet. Parasitol. 1996, 64:95-105. 10.1016/0304-4017(96)00962-4.
61. Orlofske S.A., Jadin R.C., Johnson P.T.J. It's a predator-eat-parasite world: how characteristics of predator, parasite, and environment affect consumption. Oecologia 2015, 178:537-547. 10.1007/s00442-015-3243-4.
62. Paine R.T. Food web complexity and species diversity. Am. Nat. 1966, 100(910):65-75. 10.1086/282400.
63. Paine R.T. The Pisaster-Tegula interaction: prey patches, predator food preference and intertidal community structure. Ecology 1969, 50:950-961. 10.2307/1936888.
64. Peterman J.S., Müller C.B., Weigelt A., Weisser W.W., Schmid B. Effect of plant species loss on aphid-parasitoid communities. J. Anim. Ecol. 2010, 79:709-720. 10.1111/j.1365-2656.2010.01674.x.
65. Pimm S.L., Russell G.J., Gittleman J.L., Brooks T.M. The future of biodiversity. Science 1995, 269:347-350. 10.1126/science.269.5222.347.
66. Poulin R. Evolutionary Ecology Of Parasites 2011, Princeton University Press, Princeton, New Jersey.
67. Poulin R., Morand S. The diversity of parasites. Q. Rev. Biol. 2000, 75:277-293. 10.1086/393500.
68. Poulin R., Krasnov B.R., Pilosof S., Thieltges D.W. Phylogeny determines the role of helminth parasites in intertidal food webs. J. Anim. Ecol. 2013, 82:1265-1275. 10.1111/1365-2656.12101.
69. Preston D.L., Orlofske S.A., Lambden J.P., Johnson P.T.J. Biomass and productivity of trematode parasites in pond ecosystems. J. Anim. Ecol. 2013, 82:509-517. 10.1111/1365-2656.12030.
70. Price P.W. Evolutionary Biology Of Parasites 1980, Princeton University Press, Princeton. New Jersey.
71. Råberg L., Alacid E., Garcés E., Figueroa R. The potential for Arms Race and Red Queen coevolution in a protist host-parasite system. Ecol. Evol. 2014, 4:4775-4785. 10.1002/ece3.1314.
72. Rohrlack T., Christiansen G., Kurmayer R. Putative antiparasite defense system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix. Appl. Environ. Microbiol. 2013, 79:2642-2647. 10.1128/AEM.03499-12.
73. Roopnarine P. Red Queen for a day: models of symmetry and selection in paleoecology. Evol. Ecol. 2012, 26:1-10. 10.1007/s10682-011-9494-6.
74. Roschewitz I., Hucker M., Tscharntke T., Thies C. The influence of landscape context and farming practices on parasitism of cereal aphids. Agric. Ecosyst. Environ. 2005, 108:218-227. 10.1016/j.agee.2005.02.005.
75. Rossberg A.G. Part-whole relations between food webs and the validity of local food-web descriptions. Ecol. Complex. 2008, 5:121-131. 10.1016/j.ecocom.2008.02.003.
76. Salomon P.S., Stolte W. Predicting the population dynamics in Amoebophrya parasitoids and their dinoflagellate hosts using a mathematical model. Mar. Ecol. Prog. Ser. 2010, 419:1-10. 10.3354/meps08839.
77. Schoenly K., Cohen J.E. Temporal variation in food web structure: 16 empirical cases. Ecol. Monogr. 1991, 61:267-298.
78. Sime-Ngando T. Phytoplankton chytridiomycosis: fungal parasites of phytoplankton and their imprints on the food web dynamics. Front. Microbiol. 2012, 3:361. 10.3389/fmicb.2012.00361.
79. Smith J.A., Wang Y., Wilmers C.C. Top carnivores increase their kill rates on prey as a response to human-induced fear. Proc. R. Soc. Lond. Biol. 2015, 282:20142711. 10.1098/rspb.2014.2711.
80. Stouffer D.B., Camacho J., Guimerà R., Ng A.A., Nunes Amaral L.A. Quantitative patterns in the structure of model and empirical food webs. Ecology 2005, 86:1301-1311. 10.1890/04-0957.
81. Stouffer D.B., Camacho J., Amaral L.A.N. A robust measure of food web intervality. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19015-19020. 10.1073/pnas.0603844103.
82. Sukhdeo M.V.K. Where are the parasites in food webs?. Parasit. Vectors 2012, 5:239. 10.1186/1756-3305-5-239.
83. Thieltges D.W., Reise K., Mouritsen K.N., McLaughlin J.P., Poulin R. Food web including metazoan parasites for a tidal basin in Germany and Denmark: Ecological Archives E092-172. Ecology 2011, 92:2005. 10.1890/11-0351.1.
84. Thies C., Roschewitz I., Tscharntke T. The landscape context of cereal aphid-parasitoid interactions. Proc. R. Soc. Lond. Biol. 2005, 272:203-210. 10.1098/rspb.2004.2902.
85. Thompson J.N. The Coevolutionary Process 1994, University of Chicago Press, Chicago, Illinois.
86. Thompson R.M., Mouritsen K.N., Poulin R. Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J. Anim. Ecol. 2005, 74:77-85. 10.1111/j.1365-2656.2004.00899.x.
87. Thompson R.M., Dunne J.A., Woodward G. Freshwater food webs: towards a more fundamental understanding of biodiversity and community dynamics. Freshw. Biol. 2012, 57:1329-1341. 10.1111/j.1365-2427.2012.02808.x.
88. Toft C.A. Communities of parasites with parasitic life-styles. Community Ecology 1986, 445-463. Harper & Row, New York, New York. J.M. Diamond, T.J. Case (Eds.).
89. Tylianakis J.M., Tscharntke T., Lewis O.T. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 2007, 445:202-205. 10.1038/nature05429.
90. Van Valen L. A new evolutionary law. Evol. Theory 1973, 1:1-30. http://leighvanvalen.com/evolutionary-theory/.
91. Vitousek P.M., D'Antonio C.M., Loope L.L., Rejmanek M., Westbrooks R. Introduced species: a significant component of human-caused global change. N. Z. J. Ecol. 1997, 21:1-16. http://newzealandecology.org/system/files/articles/NZJEcol21_1_1.pdf.
92. Voigt K., Marano A.V., Gleason F.H. Ecological and economical importance of parasitic zoosporic true fungi. The Mycota Vol. XI: Agricultural Applications 2013, Springer Verlag, New York, New York. second ed. F.F. Kempken (Ed.).
93. Voje K.L., Holen O.H., Liow L.H., Stenseth N.C. The role of biotic forces in driving macroevolution: beyond the Red Queen. Proc. R. Soc. B 2015, 282:50186. 10.1098/rspb.2015.0186.
94. Warren C.P., Pascual M., Lafferty K.D., Kuris A.M. The inverse niche model for food webs with parasites. Theor. Ecol. 2010, 3:285-294. 10.1007/s12080-009-0069-x.
95. Wiens J.J., Ackerly D.D., Allen A.P., Anacker B.L., Buckley L.B., Cornell H.V., Damschen E.I., Davies T.J., Grytnes J.A., Harrison S.P., Hawkins B.A., Holt R.D., McCain C.M., Stephens P.R. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol. Lett. 2010, 13:1310-1324. 10.1111/j.1461-0248.2010.01515.x.
96. Williams R.J., Martinez N.D. Simple rules yield complex food webs. Nature 2000, 404:180-183. 10.1038/35004572.
97. Williams R.J., Martinez N.D. Success and its limits among structural models of complex food webs. J. Anim. Ecol. 2008, 77:512-519. 10.1111/j.1365-2656.2008.01362.x.
98. Wolkovich E.M., Allesina S., Cottingham K.L., Moore J.C., Sandin S.A., de Mazancourt C. Linking the green and brown worlds: the prevalence of multi-channel feeding in food webs. Ecology 2014, 95:3376-3386. 10.1890/13-1721.1.
99. Wood C.L., Lafferty K.D. How have fisheries affected parasitic communities?. Parasitology 2015, 142:134-144. 10.1017/S003118201400002X.
100. Wood C.L., Lafferty K.D., Micheli F. Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 2010, 13:761-775. 10.1111/j.1461-0248.2010.01467.x.
101. Zander C.D., Josten N., Detloff K.C., Poulin R., McLaughlin J.P., Thieltges D.W. Food web including metazoan parasites for a brackish shallow water ecosystem in Germany and Denmark: ecological archives E092-174. Ecology 2011, 92:2007. 10.1890/11-0374.1.
102. Zook A.E., Eklof A., Jacob U., Allesina S. Food webs: ordering species according to body size yields high degree of intervality. J. Theor. Biol. 2011, 271:106-113. 10.1016/j.jtbi.2010.11.045.