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Parasites in food webs: the ultimate missing links

Kevin D. Lafferty, Stefano Allesina, Matias Arim and 15 more

Ecology Letters · 2008 · Review

doi:10.1111/j.1461-0248.2008.01174.x

Abstract

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food‐web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food‐web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food‐web stability, interaction strength and energy flow. Food‐web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food‐web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food‐web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.

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References 93

  1. 1.

    Anderson R, May R. Population biology of infectious diseases: Part I. Nature. 1979;280:361-367.

    Not in our library10.1038/280361a0

  2. 2.

    Anderson RM, May RM. Age-related-changes in the rate of disease transmission: implications for the design of vaccination programs. J. Hyg. 1985;94:365-436.

    Not in our library10.1017/s002217240006160x

  3. 3.

    Arim M, Marquet PA, Jaksic FM. On the relationship between productivity and food chain length at different ecological levels. Am. Nat. 2007;169:62-72.

    Not in our library10.1086/510210

  4. 4.

    Bertrand M, Marcogliese DJ, Magnan P. Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. J. Fish Biol. 2008;72:555-572.

    Not in our library

  5. 5.

    Boag B, Neilson R, Robinson D, Scrimgeour CM, Handley LL. Wild rabbit host and some parasites show trophic-level relationships for delta C-13 and delta N-15: a first report. Isotopes Environ. Health Stud. 1998;34:81-85.

    Not in our library

  6. 6.

    Borer ET. Intraguild predation in larval parasitoids: implications for coexistence. J. Anim. Ecol. 2002;71:957-965.

    Not in our library

  7. 7.

    Borer ET, Briggs CJ, Holt RD. Predators, parasitoids and pathogens: a cross-cut examination of intraguild predation theory. Ecology. 2007;88:2681-2688.

    Not in our library10.1890/06-1707.1

  8. 8.

    Brose U, Jonsson T, Berlow EL, Warren P, Banasek-Richter C, Bersier LF, et al. Consumer-resource body-size relationships in natural food webs. Ecology. 2006a;87:2411-2417.

    Not in our library10.1890/0012-9658(2006)87[2411:cbrinf]2.0.co;2

  9. 9.

    Brose U, Williams RJ, Martinez ND. Allometric scaling enhances stability in complex food webs. Ecol. Lett. 2006b;9:1228-1236.

    Not in our library10.1111/j.1461-0248.2006.00978.x

  10. 10.

    Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. Toward a metabolic theory of ecology. Ecology. 2004;85:1771-1789.

    Not in our library

  11. 11.

    Camacho J, Guimera R, Amaral LAN. Analytical solution of a model for complex food webs. Phys. Rev. E. 2002a;65.

    Not in our library10.1103/physreve.65.030901

  12. 12.

    Camacho J, Guimera R, Amaral LAN. Robust patterns in food web structure. Phys. Rev. Lett. 2002b;88.

    Not in our library10.1103/physrevlett.88.228102

  13. 13.

    Cattin MF, Bersier LF, Banasek-Richter C, Baltensperger R, Gabriel JP. Phylogenetic constraints and adaptation explain food-web structure. Nature. 2004;427:835-839.

    Not in our library10.1038/nature02327

  14. 14.

    Cohen JE, Newman CM. A stochastic-theory of community food web. 1. Models and aggregated data. Proc. R. Soc. Lond., B, Biol. Sci. 1985;224:421-448.

    Not in our library

  15. 15.

    Cohen JE, Briand F, Newman CM. Community Food Webs: Data and Theory. 1990a.

    Not in our library

  16. 16.

    Cohen JE, Luczak T, Newman CM, Zhou ZM. Stochastic structure and nonlinear dynamics of food webs – qualitative stability in a Lotka Volterra cascade model. Proc. R. Soc. Lond., B, Biol. Sci. 1990b;240:607-627.

    Not in our library

  17. 17.

    DeLeo GA, Dobson AP. Allometry and simple epidemic models for microparasites. Nature. 1996;379:720-722.

    Not in our library10.1038/379720a0

  18. 18.

    Deudero S, Pinnegar JK, Polunin NVC. Insights into fish host-parasite trophic relationships revealed by stable isotope analysis. Dis. Aquat. Org. 2002;52:77-86.

    Not in our library10.3354/dao052077

  19. 19.

    Diekmann O, Heesterbeek JAP, Metz JAJ. On the definition and the computation of the basic reproduciton ratio Ro in models for infectious-diseases in heterogenous populations. J. Math. Biol. 1990;28:365-382.

    Not in our library10.1007/bf00178324

  20. 20.

    Dobson A. Population dynamics of pathogens with multiple host species. Am. Nat. 2004;164:S64-S78.

    Not in our library10.1086/424681

  21. 21.

    Doucett RR, Giberson DJ, Power G. Parasitic association of Nanocladius (Diptera:Chironomidae) and Pteronarcys biloba (Plecoptera:Pteronarcyidae): insights from stable-isotope analysis. J. North Am. Benthol. Soc. 1999;18:514-523.

    Not in our library

  22. 22.

    Duffy MA, Hall SR, Tessier AJ, Huebner M. Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control? Limnol. Oceanogr. 2005;50:412-420.

    Not in our library

  23. 23.

    Dunne JA, Williams RJ, Martinez ND. Food-web structure and network theory: the role of connectance and size. Proc. Natl Acad. Sci. U.S.A. 2002a;99:12917-12922.

    Not in our library10.1073/pnas.192407699

  24. 24.

    Dunne JA, Williams RJ, Martinez ND. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 2002b;5:558-567.

    Not in our library

  25. 25.

    Dunne JA, Williams RJ, Martinez ND. Network structure and robustness of marine food webs. Mar. Ecol. Prog. Ser. 2004;273:291-302.

    Not in our library

  26. 26.

    Fry CH, Keith S, Urban EK. The Birds of Africa, Volume VI: Picathartes to Oxpeckers. 2000.

    Not in our library

  27. 27.

    George-Nascimento M, Munoz G, Marquet PA, Poulin R. Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecol. Lett. 2004;7:527-531.

    Not in our library

  28. 28.

    Grutter AS. Cleaner fish really do clean. Nature. 1999;398:672-673.

    Not in our library

  29. 29.

    Hughes TP. Catastrophes, phase shifts, and large scale degradation of a Caribbean coral reef. Science. 1994;265:1547-1551.

    Not in our library10.1126/science.265.5178.1547

  30. 30.

    Huspeni TC, Lafferty KD. Using larval trematodes that parasitize snails to evaluate a salt-marsh restoration project. Ecol. Appl. 2004;14:795-804.

    Not in our library

  31. 31.

    Huxham M, Raffaelli D, Pike A. Parasites and food-web patterns. J. Anim. Ecol. 1995;64:168-176.

    Not in our library

  32. 32.

    Huxham M, Beaney S, Raffaelli D. Do parasites reduce the chances of triangulation in a real food web? Oikos. 1996;76:284-300.

    Not in our library

  33. 33.

    Iken K, Brey T, Wand U, Voigt J, Junghans P. Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog. Oceanogr. 2001;50:383-405.

    Not in our library

  34. 34.

    Johnson PTJ, Carpenter SR, Ostfeld R, Keesing F, Eviner V. Influence of eutrophication on disease in aquatic ecosystems: patterns, processes, and predictions. Reciporical Interactions between Ecosystems and Disease. 2008;71-99.

    Not in our library

  35. 35.

    Kagami M, von Elert E, Ibelings BW, de Bruin A, Van Donk E. The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc. R. Soc. Lond., B, Biol. Sci. 2007;274:1561-1566.

    Not in our library10.1098/rspb.2007.0425

  36. 36.

    Kuris AM. Trophic interactions: similarity of parasitic castrators to parasitoids. Q. Rev. Biol. 1974;49:129-148.

    Not in our library

  37. 37.

    Kuris AM, Hechinger RF, Shaw JC, Whitney K, Aguirre-Macedo L, Boch C, Dobson A, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini F, Mora A, Pickering M, Talhouk N, Torchin ME, Lafferty KD. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature. 2008.

    Not in our library10.1038/nature06970

  38. 38.

    Lafferty KD. Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Mar. Ecol. Prog. Ser. 1993;96:229-237.

    Not in our library

  39. 39.

    Lafferty KD. Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitol. Today. 1997;13:251-255.

    Not in our library10.1016/s0169-4758(97)01072-7

  40. 40.

    Lafferty KD. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol. Appl. 2004;14:1566-1573.

    Not in our library

  41. 41.

    Lafferty KD, Kuris AM. Mass mortality of abalone Haliotis cracherodii on the California Channel Islands: tests of epidemiological hypotheses. Mar. Ecol. Prog. Ser. 1993;96:239-248.

    Not in our library

  42. 42.

    Lafferty KD, Kuris AM. Trophic strategies, animal diversity and body size. Trends Ecol. Evol. 2002;17:507-513.

    Not in our library

  43. 43.

    Lafferty KD, Morris AK. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology. 1996;77:1390-1397.

    Not in our library

  44. 44.

    Lafferty KD, Dobson AP, Kuris AM. Parasites dominate food web links. Proc. Natl Acad. Sci. U.S.A. 2006a;103:11211-11216.

    Not in our library10.1073/pnas.0604755103

  45. 45.

    Lafferty KD, Hechinger RF, Shaw JC, Whitney KL, Kuris AM, Collinge S, Ray C. Food webs and parasites in a salt marsh ecosystem. Disease Ecology: Community Structure and Pathogen Dynamics. 2006b;119-134.

    Not in our library

  46. 46.

    Lessios HA. Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu. Rev. Ecol. Syst. 1988;19:371-393.

    Not in our library

  47. 47.

    Marcogliese D. Food webs and biodiversity: are parasites the missing link? J. Parasitol. 2003;82(S):389-399.

    Not in our library

  48. 48.

    Marcogliese DJ, Cone DK. On the distribution and abundance of eel parasites in Nova Scotia: influence of pH. J. Parasitol. 1996;82:389-399.

    Not in our library

  49. 49.

    Marcogliese DJ, Cone DK. Food webs: a plea for parasites. Trends Ecol. Evol. 1997;12:320-325.

    Not in our library10.1016/s0169-5347(97)01080-x

  50. 50.

    Marquet PA, Quinones RA, Abades S, Labra F, Tognelli M, Arim M, et al. Scaling and power-laws in ecological systems. J. Exp. Biol. 2005;208:1749-1769.

    Not in our library10.1242/jeb.01588

  51. 51.

    Martinez ND. Artifacts or attributes – effects of resolution on the Little-Rock Lake food web. Ecol. Monogr. 1991;61:367-392.

    Not in our library

  52. 52.

    Martinez ND, Hawkins BA, Dawah HA, Feifarek BP. Effects of sampling effort on characterization of food-web structure. Ecology. 1999;80:1044-1055.

    Not in our library

  53. 53.

    May RM. Stability and Complexity in Model Ecosystems. 1973.

    Not in our library

  54. 54.

    Memmott J, Martinez ND, Cohen JE. Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. J. Anim. Ecol. 2000;69:1-15.

    Not in our library

  55. 55.

    Miner CM, Altstatt JM, Raimondi PT, Minchinton TE. Recruitment failure and shifts in community structure following mass mortality limit recovery prospects of black abalone. Mar. Ecol. Prog. Ser. 2006;327:107-117.

    Not in our library

  56. 56.

    Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S. Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc. R. Soc. Lond., B, Biol. Sci. 2006;273:1323-1328.

    Not in our library10.1098/rspb.2005.3451

  57. 57.

    Moore J. Parasites and the Behavior of Animals. 2002.

    Not in our library

  58. 58.

    Morand S, Harvey PH. Mammalian metabolism, longevity and parasite species richness. Proc. R. Soc. Lond., B, Biol. Sci. 2000;267:1999-2003.

    Not in our library10.1098/rspb.2000.1241

  59. 59.

    Mouillot D, Krasnov BR, Shenbrot GI, Poulin R. Connectance and parasite diet breadth in flea-mammal webs. Ecography. 2008;31:16-20.

    Not in our library

  60. 60.

    Mouritsen KN, Poulin R. Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. Int. J. Parasitol. 2003;33:1043-1050.

    Not in our library10.1016/s0020-7519(03)00178-4

  61. 61.

    Muller CB, Adriaanse ICT, Belshaw R, Godfray HCJ. The structure of an aphid-parasitoid community. J. Anim. Ecol. 1999;68:346-370.

    Not in our library

  62. 62.

    Neilson R, Boag B, Hartley G. Temporal host-parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses. Parasitology. 2005;131:279-285.

    Not in our library10.1017/s0031182005007717

  63. 63.

    Neutel AM, Heesterbeek JAP, de Ruiter P. Stability in real food webs: weak links in long loops. Science. 2002;296:1120-1123.

    Not in our library10.1126/science.1068326

  64. 64.

    Nunn CL, Altizer SM. The global mammal parasite database: an online resource for infectious disease records in wild primates. Evol. Anthropol. 2005;14:1-2.

    Not in our library

  65. 65.

    O’Grady SP, Dearing MD. Isotopic insight into host-endosymbiont relationships in Liolaemid lizards. Oecologia. 2006;150:355-361.

    Not in our library10.1007/s00442-006-0487-z

  66. 66.

    Ostfeld RS, Holt RD. Are predators good for your health? Evaluating evidence for top–down regulation of zoonotic disease reservoirs. Front. Ecol. Environ. 2004;2:13-20.

    Not in our library

  67. 67.

    Otto S, Rall B, Brose U. Allometric degree distributions facilitate food web stability. Nature. 2007;450:1226-1229.

    Not in our library10.1038/nature06359

  68. 68.

    Pascual M, Dunne JA, Pascual M, Dunne JA. From small to large ecological networks in a dynamic world. Ecological Networks: Linking Structure to Dynamics in Food Webs. 2006;3-24.

    Not in our library

  69. 69.

    Persson ME, Larsson P, Stenroth P. Fractionation of delta N-15 and delta C-13 for Atlantic salmon and its intestinal cestode Eubothtium crassum. J. Fish Biol. 2007;71:441-452.

    Not in our library

  70. 70.

    Pinnegar JK, Campbell N, Polunin NVC. Unusual stable isotope fractionation patterns observed for fish host-parasite trophic relationships. J. Fish Biol. 2001;59.

    Not in our library

  71. 71.

    Polis GA. Complex trophic interactions in deserts: an empirical critique of food-web theory. Am. Nat. 1991;138:123-155.

    Not in our library

  72. 72.

    Poulin R, George-Nascimento M. The scaling of total parasite biomass with host body mass. Int. J. Parasitol. 2007;37:359-364.

    Not in our library10.1016/j.ijpara.2006.11.009

  73. 73.

    Price PW. Evolutionary Biology of Parasites. 1980.

    Not in our library

  74. 74.

    Raffaelli D, Hall S, Emes C, Manly B. Constraints on body size distributions: an experimental approach using a small-scale system. Oecologia. 2000;122:389-398.

    Not in our library10.1007/s004420050045

  75. 75.

    Rott AS, Godfray HCJ. The structure of a leafminer-parasitoid community. J. Anim. Ecol. 2000;69:274-289.

    Not in our library

  76. 76.

    Schoener TW. Food webs from the small to the large. Ecology. 1989;70:1559-1589.

    Not in our library

  77. 77.

    Schotthoefer A, Labak KM, Beasley V. Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. J. Parasitol. 2007;93:1240-1243.

    Not in our library10.1645/ge1129r.1

  78. 78.

    Sinclair ARE, Sinclair ARE, Norton-Griffiths M. The eruption of the ruminants. Serengeti: Dynamics of an Ecosystem. 1979;82-103.

    Not in our library

  79. 79.

    Stouffer DB, Camacho J, Guimera R, Ng CA, Amaral LAN. Quantitative patterns in the structure of model and empirical food webs. Ecology. 2005;86:1301-1311.

    Not in our library

  80. 80.

    Stouffer DB, Camacho J, Amaral LAN. A robust measure of food web intervality. Proc. Natl Acad. Sci. U.S.A. 2006;103:19015-19020.

    Not in our library10.1073/pnas.0603844103

  81. 81.

    Stouffer DB, Camacho J, Jiang W, Amaral LAN. Evidence for the existence of a robust pattern of prey selection in food webs. Proc. R. Soc. Lond., B, Biol. Sci. 2007;274:1931-1940.

    Not in our library10.1098/rspb.2007.0571

  82. 82.

    Sumption KJ, Flowerdew JR. The ecological effects of the decline in rabbits (Oryctolagus cuniculus L) due to myxomatosis. Mammal Rev. 1985;15:151-186.

    Not in our library

  83. 83.

    Thieltges DW, Jensen KT, Poulin R. The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology. 2008.

    Not in our library10.1017/s0031182007000248

  84. 84.

    Thomas F, Poulin R. Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology. 1998;116:431-436.

    Not in our library10.1017/s003118209800239x

  85. 85.

    Thompson RM, Mouritsen KN, 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.

    Not in our library

  86. 86.

    Torchin ME, Byers JE, Huspeni TC. Differential parasitism of native and introduced snails: replacement of a parasite fauna. Biol. Invasions. 2005;7:885-894.

    Not in our library

  87. 87.

    Vazquez DP, Melian CJ, Williams NM, Bluthgen N, Krasnov BR, Poulin R. Species abundance and asymmetric interaction strength in ecological networks. Oikos. 2007;116:1120-1127.

    Not in our library

  88. 88.

    Voigt CC, Kelm DH. Host preferences of bat flies: following the bloody path of stable isotopes in a host-parasite food chain. Can. J. Zool./Rev. Can. Zool. 2006;84:397-403.

    Not in our library

  89. 89.

    Voss JD, Richardson LL. Nutrient enrichment enhances black band disease progression in corals. Coral Reefs. 2006;25:569-576.

    Not in our library

  90. 90.

    West GB, Brown JH. Constructing a theory for scaling and more – Reply. Phys. Today. 2005;58:20-21.

    Not in our library

  91. 91.

    Williams RJ, Martinez ND. Simple rules yield complex food webs. Nature. 2000;404:180-183.

    Not in our library10.1038/35004572

  92. 92.

    Williams RJ, Martinez ND. Limits to trophic levels and omnivory in complex food webs: Theory and data. Am. Nat. 2004;163:458-468.

    Not in our library10.1086/381964

  93. 93.

    Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH. Parasites alter community structure. Proc. Natl Acad. Sci. U.S.A. 2007;104:9335-9339.

    Not in our library10.1073/pnas.0700062104

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