Ecology of Parasites in Mudflat Ecosystems

  • David W. ThieltgesEmail author
  • Kim N. Mouritsen
  • Robert Poulin
Part of the Aquatic Ecology Series book series (AQEC, volume 7)


Mudflats are not only home to large numbers of bivalves, polychaetes, crustaceans, fish and birds, but also to diverse communities of parasites. In this chapter, we illustrate and explore how the resulting parasite-host interactions can affect host populations, communities and food webs in mudflat ecosystems, equalling in importance the effects resulting from other species interactions, such as predation and competition. We first give an overview of the distribution and ecology of typical parasites occurring in mudflat ecosystems. Then we illustrate the main abiotic and biotic drivers of parasite infection levels in mudflat hosts. Following this, we conceptualise and illustrate the many direct and indirect effects of parasite-host interactions on host populations, communities and food webs in mudflat ecosystems. Finally, we highlight the potential impact of ongoing global changes such as increasing temperature and species introductions on parasite-host interactions in mudflat ecosystems. With this condensed overview of the presence and ecological role of parasites in mudflat ecosystems, we hope to increase the appreciation of the manifold ecological effects of parasite-host interactions on host populations, communities and food webs of mudflat ecosystems, and to spark further research in this field.



We thank Peter Beninger and an anonymous reviewer for constructive comments on our chapter. Dörte Poszig is thanked for providing the drawings.


  1. Ambariyanto A, Seed R (1991) The infestation of Mytilus edulis Linnaeus by Polydora ciliata (Johnston) in the Conwy Estuary, North Wales. J Mollusc Stud 57:413–424CrossRefGoogle Scholar
  2. Bass D, Stentiford GD, Littlewood DTJ, Hartikainen H (2015) Diverse applications of environmental DNA methods in parasitology. Trends Parasitol 31:499–513PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bates AE, Leiterer F, Wiedeback ML, Poulin R (2011) Parasitized snails take the heat: a case of host manipulation? Oecologia 167:613–621PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bax N, Williamson A, Aquero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323CrossRefGoogle Scholar
  5. Berger VJ, Galaktionov KV, Prokofiev VV (2001) Influence of parasites on host adaptations to environmental factors: host-parasite system molluscs-trematode parthenitae. Parazitologiya 35:192–200Google Scholar
  6. Bick A (1994) Corophium volutator (Corophiidae: Amphipoda) as an intermediate host of larval Digenea – an ecological analysis in a coastal region of the southern Baltic. Ophelia 40:27–36CrossRefGoogle Scholar
  7. Blakeslee AMH, Fowler AE, Keogh CL (2013) Marine invasion and parasite escape: updates and new perspectives. Adv Mar Biol 66:87–169PubMedCrossRefPubMedCentralGoogle Scholar
  8. Buschbaum C, Buschbaum G, Schrey I, Thieltges DW (2007) Shell-boring polychaetes affect gastropod shell strength and crab predation. Mar Ecol Prog Ser 329:123–130CrossRefGoogle Scholar
  9. Cardillo M (1999) Latitude and rates of diversification in birds and butterflies. Proc R Soc B Biol Sci 266:1221–1225CrossRefGoogle Scholar
  10. Cirtwill AR, Stouffer DB (2015) Concomitant predation on parasites is highly variable but constrains the ways in which parasites contribute to food-web structure. J Anim Ecol 84:734–744PubMedPubMedCentralCrossRefGoogle Scholar
  11. Clausen KT, Larsen MH, Iversen NK, Mouritsen KN (2008) The influence of trematodes on the macroalgae consumption by the common periwinkle Littorina littorea. J Mar Biol Assoc U K 88:1481–1485CrossRefGoogle Scholar
  12. Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. The University of Chicago Press, ChicagoGoogle Scholar
  13. de Montaudouin X, Blanchet H, Bazairi H, Nazik A, Desclaux-Marchand C, Bachelet G (2016) Cockle infection by Himasthla quissetensis – II. The theoretical effect of climate change. J Sea Res 113:108–114CrossRefGoogle Scholar
  14. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  15. Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin R, Reise K, Stouffer DB, Thieltges DW, Williams RJ, Zander C-D (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biol 11:e1001579PubMedPubMedCentralCrossRefGoogle Scholar
  16. Fredensborg BL, Mouritsen KN, Poulin R (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. J Exp Mar Biol Ecol 311:253–265CrossRefGoogle Scholar
  17. Fredensborg BL, Mouritsen KN, Poulin R (2005) Impact of trematodes on host recruitment, survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Mar Ecol Prog Ser 290:109–117CrossRefGoogle Scholar
  18. Fredensborg BL, Mouritsen KN, Poulin R (2006) Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail: from small to large scale. Mar Biol 149:275–283CrossRefGoogle Scholar
  19. Galaktionov KV (2017) Patterns and processes influencing helminth parasites of Arctic coastal communities during climate change. J Helminthol 91:38–408CrossRefGoogle Scholar
  20. Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Kluwer Academic, DordrechtCrossRefGoogle Scholar
  21. Goedknegt MA, Feis ME, Wegner KM, Luttikhuizen PC, Buschbaum C, Camphuysen KCJ, van der Meer J, Thieltges DW (2016) Parasites and marine invasions: ecological and evolutionary perspectives. J Sea Res 113:11–27CrossRefGoogle Scholar
  22. Goedknegt MA, Schuster A-K, Buschbaum GR, Jung AS, Luttikhuizen PC, van der Meer J, Troost K, Wegner KM, Thieltges DW (2017) Spillover but no spillback of two invasive parasitic copepods from invasive Pacific oysters (Crassostrea gigas) to native bivalve hosts. Biol Invasions 19:365–379CrossRefGoogle Scholar
  23. Groenewold S, Berghahn R, Zander CD (1996) Parasite communities of four fish species in the Wadden Sea and the role of fish discarded by the shrimp fisheries in parasite transmission. Helgländer Meeresun 50:69–85CrossRefGoogle Scholar
  24. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  25. Gutiérrez JS, Rakhimberdiev E, Piersma T, Thieltges DW (2017) Migration and parasitism: habitat use, not migration distance, influences helminth species richness in Charadriiform birds. J Biogeogr 44:1137–1147CrossRefGoogle Scholar
  26. Harland H, MacLeod CD, Poulin R (2015) Non-linear effects of ocean acidification on the transmission of a marine intertidal parasite. Mar Ecol Prog Ser 536:55–64CrossRefGoogle Scholar
  27. Harvell D, Altizer S, Cattadori IM, Harrington L, Weil E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90:912–920PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hatcher MJ, Dunn AM (2011) Parasites in ecological communities: from interactions to ecosystems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  29. Hatcher MJ, Dick JT, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1253–1271PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hay KB, Fredensborg BL, Poulin R (2005) Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). J Mar Biol Assoc U K 85:989–992CrossRefGoogle Scholar
  31. Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc R Soc B 272:1059–1066PubMedCrossRefGoogle Scholar
  32. Hechinger RF, Lafferty KD, McLaughlin JP, Fredensborg BL, Huspeni TC, Lorda J, Sandhu PK, Shaw JC, Torchin ME, Whitney KL, Kuris AM (2011) Food webs including parasites, biomass, body sizes, and life stages for three California/Baja California estuaries. Ecology 92:791CrossRefGoogle Scholar
  33. Høeg JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J Mar Biol Assoc U K 75:517–550CrossRefGoogle Scholar
  34. Høeg JT, Lützen J (1995) Life cycle and reproduction in the Cirripedia Rhizocephala. Oceanogr Mar Biol Annu Rev 33:427–485Google Scholar
  35. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528PubMedCrossRefGoogle Scholar
  36. Hopper JV, Poulin R, Thieltges DW (2008) Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. J Exp Mar Biol Ecol 367:153–156CrossRefGoogle Scholar
  37. Horn MH, Martin KLM, Chotkowski MA (1999) Intertidal fishes: life in two worlds. Academic Press, LondonGoogle Scholar
  38. Huxham M, Raffaelli D, Pike A (1993) The influence of Cryptocotyle lingua (Digenea: Plathyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prosobranchia); an ecological approach. J Exp Mar Biol Ecol 168:223–238CrossRefGoogle Scholar
  39. Jensen KT (1993) Density-dependent growth in cockles (Cerastoderma edule): evidence from interannual comparisons. J Mar Biol Assoc U K 73:333–342CrossRefGoogle Scholar
  40. Jensen KT, Mouritsen KN (1992) Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator – the possible role of trematodes. Helgoländer Meeresun 46:329–339CrossRefGoogle Scholar
  41. Jensen KT, Latama G, Mouritsen KN (1996) The effect of larval trematodes on the survival rates of two species of mud snails (Hydrobiidae) experimentally exposed to desiccation, freezing and anoxia. Helgoländer Meeresun 50:327–335CrossRefGoogle Scholar
  42. Jensen T, Jensen KT, Mouritsen KN (1998) The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival. J Exp Mar Biol Ecol 227:35–48CrossRefGoogle Scholar
  43. Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol 213:961–970PubMedCrossRefGoogle Scholar
  44. 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 25:362–371PubMedCrossRefGoogle Scholar
  45. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  46. Kaiser MJ, Attrill MJ, Jennings S, Thomas DN, Barnes DKA (2011) Marine ecology: processes, systems, and impacts. Oxford University Press, OxfordGoogle Scholar
  47. Kamiya T, O'Dwyer K, Nakagawa S, Poulin R (2014) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biol Rev 89:123–134PubMedCrossRefGoogle Scholar
  48. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2205PubMedCrossRefGoogle Scholar
  49. Kent RML (1981) The effect of Polydora ciliata on the shell strength of Mytilus edulis. J Cons Int Explor Mer 39:252–255CrossRefGoogle Scholar
  50. Koch W, Boer P, Witte JIJ, van der Veer HW, Thieltges DW (2014) Inventory and comparison of abundance of parasitic copepods on fish hosts in the western Wadden Sea (North Sea) between 1968 and 2010. J Mar Biol Assoc U K 94:547–555CrossRefGoogle Scholar
  51. Koehler AV, Poulin R (2010) Host partitioning by parasites in an intertidal crustacean community. J Parasitol 96:862–868PubMedCrossRefPubMedCentralGoogle Scholar
  52. Koprivnikar J, Lim D, Fu C, Brack SHM (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitol Res 106:1167–1177PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518PubMedCrossRefGoogle Scholar
  54. Lafferty KD (1993) Effect of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Mar Ecol Prog Ser 96:229–237CrossRefGoogle Scholar
  55. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513CrossRefGoogle Scholar
  56. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35:31–54CrossRefGoogle Scholar
  57. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546PubMedPubMedCentralCrossRefGoogle Scholar
  58. Larsen MH, Mouritsen KN (2009) Increasing temperature counteracts the impact of parasitism on periwinkle consumption. Mar Ecol Prog Ser 383:141–149CrossRefGoogle Scholar
  59. Larsen MH, Mouritsen KN (2014) Temperature–parasitism synergy alters intertidal soft-bottom community structure. J Exp Mar Biol Ecol 460:109–119CrossRefGoogle Scholar
  60. Larsen MH, Jensen KT, Mouritsen KN (2011) Climate influences parasite-mediated competitive release. Parasitology 138:1436–1441PubMedCrossRefGoogle Scholar
  61. Latham ADM, Poulin R (2002) New records of gastrointestinal helminths from the southern black-backed gull (Larus dominicanus) in New Zealand. N Z J Zool 29:253–257CrossRefGoogle Scholar
  62. Lauckner G (1980) Diseases of mollusca: gastropoda. In: Kinne O (ed) Diseases of marine animals, General aspects, protozoa to gastropoda, vol I. Wiley, New York, pp 311–424Google Scholar
  63. Lauckner G (1983) Diseases of mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals, Introduction, Bivalvia to Scaphopoda, vol 2. Biologische Anstalt Helgoland, Hamburg, pp 477–961Google Scholar
  64. Lei F, Poulin R (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Mar Biol 158:995–1003CrossRefGoogle Scholar
  65. Leung TLF, Donald KM, Keeney DB, Koehler AV, Peoples RC, Poulin R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. N Z J Mar Freshw Res 43:857–865CrossRefGoogle Scholar
  66. MacLeod CD, Poulin R (2012) Host–parasite interactions: a litmus test for ocean acidification? Trends Parasitol 28:365–369PubMedCrossRefGoogle Scholar
  67. MacLeod CD, Poulin R (2015) Differential tolerances to ocean acidification by parasites that share the same host. Int J Parasitol 45:485–493PubMedCrossRefGoogle Scholar
  68. MacLeod CD, Poulin R (2016) Parasitic infection alters the physiological response of a marine gastropod to ocean acidification. Parasitology 143:1397–1408PubMedCrossRefGoogle Scholar
  69. McCurdy DG, Forbes MR, Boates JS (1999) Testing alternative hypotheses for variation in amphipod behaviour and life history in relation to parasitism. Int J Parasitol 29:1001–1009PubMedCrossRefPubMedCentralGoogle Scholar
  70. McDaniel JS (1969) Littorina littorea: lowered heat tolerance due to Cryptocotyle lingua. Exp Parasitol 25:13–15PubMedCrossRefPubMedCentralGoogle Scholar
  71. Meissner K, Bick A (1997) Population dynamics and ecoparasitological surveys of Corophium volutator in coastal waters in the Bay of Mecklenburg (southern Baltic Sea). Dis Aquat Org 29:169–179CrossRefGoogle Scholar
  72. Meissner K, Bick A (1999) Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae) ± laboratory studies. Dis Aquat Org 35:47–52CrossRefGoogle Scholar
  73. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA, Bange HW, Hansen HP, Körtzinger A (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160:1875–1888CrossRefGoogle Scholar
  74. Morley NJ (2011) Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138:1442–1452PubMedCrossRefPubMedCentralGoogle Scholar
  75. Morley NJ (2012) Thermodynamics of miracidial survival and metabolism. Parasitology 139:1640–1651PubMedCrossRefPubMedCentralGoogle Scholar
  76. Morley NJ, Lewis JW (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140:1211–1224PubMedCrossRefPubMedCentralGoogle Scholar
  77. Morley NJ, Lewis JW (2015) Thermodynamics of trematode infectivity. Parasitology 142:585–597PubMedCrossRefPubMedCentralGoogle Scholar
  78. Mouritsen KN (2002a) The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J Helminthol 76:341–347PubMedCrossRefPubMedCentralGoogle Scholar
  79. Mouritsen KN (2002b) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124:521–528PubMedPubMedCentralGoogle Scholar
  80. Mouritsen KN, Haun SCB (2008) Community regulation by herbivore parasitism and density: trait-mediated indirect interactions in the intertidal. J Exp Mar Biol Ecol 367:236–246CrossRefGoogle Scholar
  81. Mouritsen KN, Jensen KT (1994) The enigma of gigantism: effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 181:53–66CrossRefGoogle Scholar
  82. Mouritsen KN, Jensen KT (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Mar Ecol Prog Ser 151:123–134CrossRefGoogle Scholar
  83. Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117PubMedPubMedCentralGoogle Scholar
  84. Mouritsen KN, Poulin R (2005) Parasite boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos 108:344–350CrossRefGoogle Scholar
  85. Mouritsen KN, Poulin R (2006) A parasite indirectly impacts both abundance of primary producers and biomass of secondary producers in an intertidal benthic community. J Mar Biol Assoc U K 86:221–226CrossRefGoogle Scholar
  86. Mouritsen KN, Mouritsen LT, Jensen KT (1998) Changes of topography and sediment characteristics on an intertidal mud-fat following mass-mortality of the amphipod Corophium volutator. J Mar Biol Assoc U K 78:1167–1180CrossRefGoogle Scholar
  87. Mouritsen KN, Gorbushin A, Jensen KT (1999) Influence of trematode infections on in situ growth rates of Littorina littorea. J Mar Biol Assoc U K 79:425–430CrossRefGoogle Scholar
  88. Mouritsen KN, McKechnie S, Meenken E, Toynbee JL, Poulin R (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. J Mar Biol Assoc U K 83:307–310CrossRefGoogle Scholar
  89. Mouritsen KN, Tompkins DM, Poulin R (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146:476–483PubMedCrossRefPubMedCentralGoogle Scholar
  90. Mouritsen KN, Poulin R, McLaughlin JP, Thieltges DW (2011) Food web including metazoan parasites for an intertidal ecosystem in New Zealand. Ecological Archives E092–173. Ecology 92:2006CrossRefGoogle Scholar
  91. O’Connell-Milne SA, Poulin R, Savage C, Rayment W (2016) Reduced growth, body condition and foot length of the bivalve Austrovenus stutchburyi in response to parasite infection. J Exp Mar Biol Ecol 474:23–28CrossRefGoogle Scholar
  92. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RE, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686PubMedCrossRefPubMedCentralGoogle Scholar
  93. Pechenik JA, Fried B, Simpkins HL (2001) Crepidula fornicata is not a first intermediate host for trematodes: who is? J Exp Mar Biol Ecol 261:211–224PubMedCrossRefPubMedCentralGoogle Scholar
  94. Peoples RC (2013) A review of the helminth parasites using polychaetes as hosts. Parasitol Res 112:3409–3421PubMedCrossRefPubMedCentralGoogle Scholar
  95. Peoples RC, Randhawa HS, Poulin R (2012) Parasites of polychaetes and their impact on host survival in Otago Harbour, New Zealand. J Mar Biol Assoc U K 92:449–455CrossRefGoogle Scholar
  96. Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151PubMedCrossRefPubMedCentralGoogle Scholar
  97. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, PrincetonGoogle Scholar
  98. Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study Behav 41:151–186CrossRefGoogle Scholar
  99. Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18:176–183PubMedCrossRefPubMedCentralGoogle Scholar
  100. Poulin R, Mouritsen KN (2003) Large-scale determinants of trematode infections in intertidal gastropods. Mar Ecol Prog Ser 254:187–198CrossRefGoogle Scholar
  101. Poulin R, Mouritsen KN (2006) Climate change, parasitism and the structure of intertidal ecosystems. J Helminthol 80:183–191PubMedCrossRefPubMedCentralGoogle Scholar
  102. Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390PubMedCrossRefPubMedCentralGoogle Scholar
  103. Probst S, Kube J (1999) Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia ventrosa (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 238:49–68CrossRefGoogle Scholar
  104. Raffaelli D, Hawkins SJ (1999) Intertidal ecology. Springer, BerlinGoogle Scholar
  105. Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618PubMedCrossRefPubMedCentralGoogle Scholar
  106. Reise K (1985) Tidal flat ecology. Springer, BerlinCrossRefGoogle Scholar
  107. Rhode K (1993) Ecology of marine parasites: an introduction to marine parasitology. CAB International, WallingfordGoogle Scholar
  108. Rhode K (ed) (2005) Marine parasitology. CSIRO Publishing, Melbourne and WallingfordGoogle Scholar
  109. Riel A (1975) Effect of trematodes on survival of Nassarius obsoletus (Say). Proc Malacol Soc Lond 41:527–528Google Scholar
  110. Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, OxfordGoogle Scholar
  111. Seaman B, Briffa M (2015) Parasites and personality in periwinkles (Littorina littorea): infection status is associated with mean-level boldness but not repeatability. Behav Process 115:132–134CrossRefGoogle Scholar
  112. Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111:S111–S127PubMedCrossRefPubMedCentralGoogle Scholar
  113. Sokolova IM (1995) Influence of trematodes on the demography of Littorina saxatilis (Gastropoda: Prosobranchia: Littorinidae) in the White Sea. Dis Aquat Org 21:91–101CrossRefGoogle Scholar
  114. Solomon S, Quinn D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) (2007) Climate change 2007: the physical science basis: contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  115. Sousa WP, Gleason M (1989) Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda : Prosobranchia). Oecologia 80:456–464PubMedCrossRefPubMedCentralGoogle Scholar
  116. Stier T, Drent J, Thieltges DW (2015) Trematode infections reduce clearance rates and condition in blue mussels Mytilus edulis. Mar Ecol Prog Ser 529:137–144CrossRefGoogle Scholar
  117. Studer A, Poulin R (2012) Seasonal dynamics in an intertidal mudflat: the case of a complex trematode life cycle. Mar Ecol Prog Ser 455:79–93CrossRefGoogle Scholar
  118. Studer A, Poulin R (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitol Res 112:243–249PubMedCrossRefPubMedCentralGoogle Scholar
  119. Studer A, Thieltges DW, Poulin R (2010) Parasites and global warming: the net effect of temperature on an intertidal host-parasite system. Mar Ecol Prog Ser 415:11–22CrossRefGoogle Scholar
  120. Studer A, Poulin R, Tompkins DM (2013a) Local effects of a global problem: modelling the risk of parasite-induced mortality in an intertidal trematode-amphipod system. Oecologia 172:1213–1222PubMedCrossRefPubMedCentralGoogle Scholar
  121. Studer A, Widmann M, Poulin R, Krkošek M (2013b) Large scale patterns of trematode parasitism in a bivalve host: no evidence for a latitudinal gradient in infection levels. Mar Ecol Prog Ser 491:125–135CrossRefGoogle Scholar
  122. Tallmark B, Norrgren G (1976) The influence of parasitic trematodes on the ecology of Nassarius reticulatus (L.) in Gullmar Fjord (Sweden). Zoon 4:149–154Google Scholar
  123. Thieltges DW (2006a) Parasite induced summer mortality in common cockles Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559:455–461CrossRefGoogle Scholar
  124. Thieltges DW (2006b) Effect of infection by the metacercarial trematode Renicola roscovita on growth in intertidal blue mussel Mytilus edulis. Mar Ecol Prog Ser 319:129–134CrossRefGoogle Scholar
  125. Thieltges DW (2007) Habitat and transmission – effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve. Parasitology 134:599–605PubMedCrossRefPubMedCentralGoogle Scholar
  126. Thieltges DW (2008) Effect of host size and exposure on metacercarial infection levels in the intertidal cockle Cerastoderma edule. J Mar Biol Assoc U K 88:613–616CrossRefGoogle Scholar
  127. Thieltges DW, Poulin R (2016) Food-web-based comparison of the drivers of helminth parasite species richness in coastal fish and bird definitive hosts. Mar Ecol Prog Ser 545:9–19CrossRefGoogle Scholar
  128. Thieltges DW, Reise K (2007) Spatial heterogeneity in parasite infections at different scales in an intertidal bivalve. Oecologia 150:569–581PubMedCrossRefPubMedCentralGoogle Scholar
  129. Thieltges DW, Rick J (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Dis Aquat Org 73:63–68PubMedCrossRefPubMedCentralGoogle Scholar
  130. Thieltges DW, Krakau M, Andresen H, Fottner S, Reise K (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgol Mar Res 60:307–316CrossRefGoogle Scholar
  131. Thieltges DW, Jensen KT, Poulin R (2008a) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426PubMedPubMedCentralGoogle Scholar
  132. Thieltges DW, Donas-Botto Bordalo M, Hernández C, Prinz K, Jensen KT (2008b) Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135:1111–1116PubMedPubMedCentralGoogle Scholar
  133. Thieltges DW, de Montaudouin X, Fredensborg BL, Jensen KT, Koprivnikar J, Poulin R (2008c) Production of marine trematode cercariae – a potentially overlooked path of energy flow in benthic systems. Mar Ecol Prog Ser 372:147–155CrossRefGoogle Scholar
  134. Thieltges DW, Ferguson MAD, Jones CS, Noble LR, Poulin R (2009a) Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe. J Biogeogr 36:1493–1501CrossRefGoogle Scholar
  135. Thieltges DW, Fredensborg BL, Poulin R (2009b) Geographical variation in metacercarial infection levels in marine invertebrate hosts–parasite species character versus local factors. Mar Biol 156:983–990CrossRefGoogle Scholar
  136. Thieltges DW, Fredensborg BL, Studer A, Poulin R (2009c) Large-scale patterns in trematode richness and infection levels in marine crustacean hosts. Mar Ecol Prog Ser 389:139–147CrossRefGoogle Scholar
  137. Thieltges DW, Reise K, Jensen KT (2009d) Invaders interfere with native parasite-host interactions. Biol Invasions 11:1421–1429CrossRefGoogle Scholar
  138. Thieltges DW, Saldanha I, Leung TLF, Poulin R (2009e) Contribution of parasites to intra- and inter-site variation in shell morphology of a marine gastropod. J Mar Biol Assoc U K 89:563–568CrossRefGoogle Scholar
  139. Thieltges DW, Reise K, Mouritsen KN, McLaughlin JP, Poulin R (2011) Food web including metazoan parasites for a tidal basin in Germany and Denmark. Ecological Archives E092–172. Ecology 92:2005CrossRefGoogle Scholar
  140. Thieltges DW, Engelsma MY, Wendling CC, Wegner KM (2013a) Parasites in the Wadden Sea food web. J Sea Res 82:122–133CrossRefGoogle Scholar
  141. Thieltges DW, Amundsen P-A, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander C-D, Poulin R (2013b) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482Google Scholar
  142. Thomas F, Poulin R (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116:431–436PubMedCrossRefGoogle Scholar
  143. Thomas F, Poulin R, de Meeus T, Guegan J-F, Renaud F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84:167–171CrossRefGoogle Scholar
  144. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefPubMedCentralGoogle Scholar
  145. Torchin ME, Miura O, Hechinger RFG (2015) Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts. Ecology 96:3033–3042PubMedCrossRefPubMedCentralGoogle Scholar
  146. Turner JRG, Gatehouse CM, Corey CA (1987) Does solar-energy control organic diversity—butterflies, moths and the British climate. Oikos 48:195–205CrossRefGoogle Scholar
  147. Wegeberg AM, Jensen KT (1999) Reduced survivorship of Himasthla (Trematoda, Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. J Sea Res 42:325–331CrossRefGoogle Scholar
  148. Wegeberg AM, Jensen KT (2003) In situ growth of juvenile cockles, Cerastoderma edule, experimentally infected with larval trematodes (Himasthla interrupta). J Sea Res 50:37–43CrossRefGoogle Scholar
  149. Welsh JE, van der Meer J, Brussaard CPD, Thieltges DW (2014) Inventory of organisms interfering with transmission of a marine trematode. J Mar Biol Assoc U K 94:697–702CrossRefGoogle Scholar
  150. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu Rev Ecol Evol Syst 34:273–309CrossRefGoogle Scholar
  151. Wilson WH (1991) Competition and predation in marine soft-sediment communities. Annu Rev Ecol Syst 21:221–241CrossRefGoogle Scholar
  152. Zander CD, Josten N, Detloff KC, Poulin R, McLaughlin JP, Thieltges DW (2011) Food web including metazoan parasites for a brackish shallow water ecosystem in Germany and Denmark. Ecological Archives E092–174. Ecology 92:2007CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • David W. Thieltges
    • 1
    Email author
  • Kim N. Mouritsen
    • 2
  • Robert Poulin
    • 3
  1. 1.Department of Coastal SystemsNIOZ Royal Netherlands Institute for Sea Research, and Utrecht UniversityDen BurgThe Netherlands
  2. 2.Department of Bioscience, Marine EcologyUniversity of AarhusAarhusDenmark
  3. 3.Department of ZoologyUniversity of OtagoDunedinNew Zealand

Personalised recommendations