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International Journal of Biometeorology

, Volume 55, Issue 6, pp 805–817 | Cite as

A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems

  • Alison DonnellyEmail author
  • Amelia Caffarra
  • Bridget F. O’Neill
Original Paper

Abstract

Mismatches in phenology between mutually dependent species, resulting from climate change, can have far-reaching consequences throughout an ecosystem at both higher and lower trophic levels. Rising temperatures, due to climate warming, have resulted in advances in development and changes in behaviour of many organisms around the world. However, not all species or phenophases are responding to this increase in temperature at the same rate, thus creating a disruption to previously synchronised interdependent key life-cycle stages. Mismatches have been reported between plants and pollinators, predators and prey, and pests and hosts. Here, we review mismatches between interdependent phenophases at different trophic levels resulting from climate change. We categorized the studies into (1) terrestrial (natural and agricultural) ecosystems, and (2) aquatic (freshwater and marine) ecosystems. As expected, we found reports of ‘winners’ and ‘losers’ in each system, such as earlier emergence of prey enabling partial avoidance of predators, potential reductions in crop yield if herbivore pests emerge before their predators and possible declines in marine biodiversity due to disruption in plankton-fish phenologies. Furthermore, in the marine environment rising temperatures have resulted in synchrony in a previously mismatched prey and predator system, resulting in an abrupt population decline in the prey species. The examples reviewed suggest that more research into the complex interactions between species in terrestrial and aquatic ecosystems is necessary to make conclusive predictions of how climate warming may impact the fragile balances within ecosystems in future.

Keywords

Phenology Terrestrial Marine Freshwater Agricultural ecosystems 

Notes

Acknowledgements

The Irish Environmental Protection Agency (EPA) funded this work under the STRIVE programme, project number 2007-CCRP-2.4, Climate change impacts on phenology: implications for terrestrial ecosystems. The authors would like to express their gratitude to the reviewers for their helpful comments and thorough consideration, which greatly enhanced an earlier draft of this paper.

References

  1. Adrian R, Wilhelm S, Gerten D (2006) Life-history traits of lake plankton species may govern their phenological response to climate warming. Glob Change Biol 12:652–661CrossRefGoogle Scholar
  2. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MS, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16CrossRefGoogle Scholar
  3. Berger SA, Diehl S, Stibor H, Trommer G, Ruhenstroth M (2010) Water temperature and stratification depth independently shift cardinal events during plankton spring succession. Glob Change Biol 16:1954–1965CrossRefGoogle Scholar
  4. Both C (2010) Food availability, mistiming and climate change. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, UK, pp 129–147Google Scholar
  5. Both C, van Asch M, Bijksma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations. J Anim Ecol 78:73–83CrossRefGoogle Scholar
  6. Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc Lond B 227:1259–1266CrossRefGoogle Scholar
  7. Carroll DP, Hoyt SC (1984) Natural enemies and their effects on apple aphid, Aphis pomi DeGeer (Homoptera: Aphididae), colonies on young apple trees in central Washington. Environ Entomol 15:607–613Google Scholar
  8. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803CrossRefGoogle Scholar
  9. Costello JH, Sullivan BK, Gifford DJ (2006) A physical-biological interaction underlying variable phenological responses to climate change by coastal zooplankton. J Plankton Res 28:1099–1105CrossRefGoogle Scholar
  10. Dawson A (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos Trans R Soc Lond B 363:1621–1633CrossRefGoogle Scholar
  11. Deneke R, Nixdorf B (1999) On the occurrence of clear-water phases in relation to shallowness and trophic state: a comparative study. Hydrobiologia 408(409):251–262CrossRefGoogle Scholar
  12. Doi H, Gordo O, Katano I (2008) Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Clim Res 36:181–190CrossRefGoogle Scholar
  13. Donnelly A, Salamin N, Jones MB (2006) Changes in tree phenology: an indicator of spring warming in Ireland? Biol Environ 106:47–55Google Scholar
  14. Donnelly A, Cooney T, Jennings E, Buscardo E, Jones MB (2009) Response of birds to climatic variability; evidence from the western fringe of Europe. Int J Biometeorol 53:211–220CrossRefGoogle Scholar
  15. Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283CrossRefGoogle Scholar
  16. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefGoogle Scholar
  17. Ficke A, Gadoury DM, Seem RC, Dry IB (2003) Effects of ontogenic resistance upon establishment and growth of Uncinula necator on grape berries. Phytopathology 93:556–563CrossRefGoogle Scholar
  18. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691CrossRefGoogle Scholar
  19. Gaedke U, Ruhenstroth-Bauer M, Wiegand I, Tirok K, Aberle N, Breithaupt P, Lengfellner K, Wohlers J, Sommer U (2010) Biotic interactions may overrule direct climate effects on spring phytoplankton dynamics. Glob Change Biol 16:1122–1136CrossRefGoogle Scholar
  20. Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE (2006) Climate change effects on plant disease: Genomes to ecosystems. Annu Rev Phytopathol 44:489–509CrossRefGoogle Scholar
  21. Garrett KA, Nita M, De Wolf ED, Gomez L Sparks AH (2009) Plant pathogens as indicators of climate change. In: Letcher T (ed) Climate and global change: observed impacts on Planet Earth. Elsevier, New York, pp 425–437Google Scholar
  22. Gomi T, Nagasaka M, Fukuda T, Hagihara H (2007) Shifting of the life cycle and life-history traits of the fall webworm in relation to climate change. Entomol Exp Appl 125:179–184CrossRefGoogle Scholar
  23. Gomi T, Adachi K, Shimizu A, Tanimoto K, Kawabata E, Takeda M (2009) Northerly shift in voltinism watershed in Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) along the Japan Sea coast: evidence of global warming? Appl Entomol Zool 44:357–362CrossRefGoogle Scholar
  24. Gordo O (2007) Why are bird migration dates shifting? A review of weather and climate effects on avian migratory phenology. Clim Res 35:37–58CrossRefGoogle Scholar
  25. Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495CrossRefGoogle Scholar
  26. Gordo O, Sanz JJ (2006) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecol Entomol 31:261–268CrossRefGoogle Scholar
  27. Gordo O, Sanz JJ (2009) Long-term temporal changes of plant phenology in the Western Mediterranean. Glob Change Biol 15:1930–1948CrossRefGoogle Scholar
  28. Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Glob Change Biol 16:1082–1106CrossRefGoogle Scholar
  29. Grabenweger G, Hopp H, Jackel B, Balder H, Koch T, Schmolling S (2007) Impact of poor host-parasitoid synchronisation on the parasitism of Cameraria ohridella (Lepidoptera: Gracillariidae). Eur J Entomol 104:153–158Google Scholar
  30. Gregory PJ, Johnson SN, Newton AC, Ingram JSI (2009) Integrating pests and pathogens into the climate change/food security debate. J Exp Bot 60:2827–2838CrossRefGoogle Scholar
  31. Hampton SE, Romare P, Seiler DE (2006) Environmentally controlled Daphnia spring increase with implications for sockeye salmon fry in Lake Washington, USA. J Plankton Res 28:399–406CrossRefGoogle Scholar
  32. Harrington R, Woiwod I, Sparks T (1999) Climate change and trophic interactions. Trends Ecol Evol 14:146–150CrossRefGoogle Scholar
  33. Hastings PJ, Bull HJ, Klump JR, Rosenberg SM (2000) Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103:723–731CrossRefGoogle Scholar
  34. Hegland SJ, Nielsen A, Lázaro A, Bjerknes A, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195CrossRefGoogle Scholar
  35. Hoover JK, Newman JA (2004) Tritrophic interactions in the context of climate change: a model of grasses, cereal aphids and their parasitoids. Glob Change Biol 10:1197–1208CrossRefGoogle Scholar
  36. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97:1630–1633CrossRefGoogle Scholar
  37. Jones GV, Davis RE (2000) Climate influences on grapevine phenology, grape composition, and wine production and quality for Bordeaux, France. Am J Enol Vitic 51:249–261Google Scholar
  38. Kahru M, Brotas V, Manzano-Sarabia M, Mitchell BG (2010) Are phytoplankton blooms occurring earlier in the Arctic? Glob Change Biol (in press)Google Scholar
  39. Katan J (2000) Physical and cultural methods for the management of soil-borne pathogens. Crop Prot 19:725–731CrossRefGoogle Scholar
  40. Koch MF, Mew TW (1991) Effects of plant age and leaf maturity on the quantitative resistance of rice cultivars to Xanthomonas campestris pv. oryzae. Plant Dis 75:901–904CrossRefGoogle Scholar
  41. Laštůvka Z (2009) Climate change and its possible influence on the occurrence and importance of insect pests. Plant Prot Sci 45:53–62Google Scholar
  42. Lehikoinen E, Sparks TH (2010) Changes in migration. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, pp 89–112Google Scholar
  43. Lyon BE, Chaine AS, Winkler DW (2008) A matter of timing. Science 321:1051–1052CrossRefGoogle Scholar
  44. Mackas DL, Batten S, Trudel M (2007) Effects on zooplankton of a warmer ocean: recent evidence from the Pacific Northwest. Prog Oceanogr 75:223–252CrossRefGoogle Scholar
  45. Martín-Vertedor D, Ferrero-García JJ, Torres-Vila LM (2010) Global warming affects phenology and voltinism of Lobesia botrana in Spain. Agric For Entomol 12:169–176CrossRefGoogle Scholar
  46. Matthysen E, Adriaensen F, Dhondt AA (2011) Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus, Parus major). Glob Change Biol 17:1–6CrossRefGoogle Scholar
  47. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 1:710–717CrossRefGoogle Scholar
  48. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissolli P, Braslavská O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen R, Remišová V, Scheifinger H, Striz M, Suskin A, van Vliet AJH, Wielgolaski FE, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1–8CrossRefGoogle Scholar
  49. Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau's Concord: a community perspective. Ecology 89:332–341CrossRefGoogle Scholar
  50. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc Lond B 365:3177–3186CrossRefGoogle Scholar
  51. Moreno-Ostos E, Paracuellos M, de Vicente I, Nevado JC, Cruz-Pizarro L (2008) Response of waterbirds to alternating clear and turbid water phases in two shallow Mediterranean lakes. Aquat Ecol 42:701–706CrossRefGoogle Scholar
  52. Musolin DL, Tougou D, Fujisaki K (2010) Too hot to handle? Phenological and life-history responses to simulated climate change of the southern green stink bug Nezara viridula (Heteroptera: Pentatomidae). Glob Change Biol 16:37–38CrossRefGoogle Scholar
  53. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  54. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872CrossRefGoogle Scholar
  55. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  56. Pavan F, Floreani C, Barro P, Zandigiacomo P, Dalla Montà L (2010) Influence of Generation and Photoperiod on Larval Development of Lobesia botrana (Lepidoptera: Tortricidae). Environ Entomol 39:1652–1658CrossRefGoogle Scholar
  57. Peñuelas J, Filella I (2001) Responses to a warming world. Science 294:793–795CrossRefGoogle Scholar
  58. Ponti L, Cossu QA, Gutierrez AP (2009) Climate warming effects on the Olea europaea–Bactrocera oleae system in Mediterranean islands: Sardinia as an example. Glob Change Biol 15:2874–2884CrossRefGoogle Scholar
  59. Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Trans R Soc Lond B 363:2369–2375CrossRefGoogle Scholar
  60. Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integr Zool 5:132–142CrossRefGoogle Scholar
  61. Root TL, Price JT, Schneider SH, Rosenzweig D, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefGoogle Scholar
  62. Roy DB, Sparks TH (2000) Phenology of British butterflies and climate change. Glob Change Biol 6:407–416CrossRefGoogle Scholar
  63. Sadras VO, Monzon JP (2006) Modelled wheat phenology captures rising temperature trends: shortened time to flowering and maturity in Australia and Argentina. Field Crops Res 99:136–146CrossRefGoogle Scholar
  64. Satake A, Ohgushi T, Urano S, Uchimura K (2006) Modelling population dynamics of a tea pest with temperature-dependent development: predicting emergence timing and potential damage. Ecol Res 21:107–116CrossRefGoogle Scholar
  65. Schlüter MH, Merico A, Reginatto M, Boersma M, Wiltshire KH, Greves W (2010) Phenological shifts of three interacting zooplankton groups in relation to climate change. Glob Change Biol 16:3144–3153Google Scholar
  66. Seebens H, Einsle U, Straile D (2009) Copepod life cycle adaptations and success in response to phytoplankton spring bloom phenology. Glob Change Biol 15:1394–1404CrossRefGoogle Scholar
  67. Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos Trans R Soc Lond B 365:3161–3176CrossRefGoogle Scholar
  68. Søreide JA, Leu E, Berge J, Graeve M, Falk-Petersen S (2010) Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Glob Change Biol 16:3154–3163Google Scholar
  69. Sparks TH, Yates TJ (1997) The effect of spring temperature on the appearance dates of British butterflies 1883–1993. Ecography 20:368–374CrossRefGoogle Scholar
  70. Sparks TH, Bairlein F, Bojarinova JG, Huppop O, Lehikoinen EA, Rainio K, Sokolov LV, Walker D (2005) Examining the total arrival distribution of migratory birds. Glob Change Biol 11:22–30CrossRefGoogle Scholar
  71. Stabentheiner A (2001) Thermoregulation of dancing bees: thoracic temperature of pollen and nectar foragers in relation to profitability of foraging and colony need. J Insect Physiol 47:385–392CrossRefGoogle Scholar
  72. Stabentheiner A, Kovac H, Brodschneider R (2010) Honeybee colony thermoregulation – regulatory mechanisms and contribution of individuals in dependence on age. Location and thermal stress. PLoS ONE 5:e8967. doi: 10.1371/journal.pone.0008967 CrossRefGoogle Scholar
  73. Stefanescu C, Peñuelas J, Filella I (2003) Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Glob Change Biol 9:1494–1506CrossRefGoogle Scholar
  74. Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life-history traits: non-linearity and match-mismatch to the environment. Proc Natl Acad Sci USA 99:13379–13381CrossRefGoogle Scholar
  75. Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Chan K, Lima M (2002) Ecological effects of climate fluctuations. Science 23:1292–1296CrossRefGoogle Scholar
  76. Stireman JO, Dyer LA, Janzen DH, Singer MS, Lill JT, Marquis RJ, Ricklets RE, Gentry GL, Hallwachs W, Coley PD, Barone JA, Greeney HF, Connahs H, Barbosa P, Morais HC, Diniz IR (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. Proc Natl Acad Sci USA 102:17384–17387CrossRefGoogle Scholar
  77. Thackeray SJ, Jones ID, Maberly SC (2008) Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climate change. J Ecol 96:523–535CrossRefGoogle Scholar
  78. Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Caravalho L, Clutton-Brock T, Dawson A, Edwards M, Elliott JM, Harrington R, Johns D, Jones ID, Jones JT, Leech DI, Roy DB, Scott WA, Smith M, Smithers RJ, Winfield IJ, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial ecosystems. Glob Change Biol 16:3304–3313CrossRefGoogle Scholar
  79. Thomson SV (2000) Epidemiology of fire blight. In: Vanneste JL (ed) Fire blight the disease and its causative agent, Erwinia amylovora. CABI Publishing, Wallingford, UK, pp 9–36CrossRefGoogle Scholar
  80. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering genophyte. Proc R Soc Lond B 365:3187–3199Google Scholar
  81. Tikkanen O-P, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operpphtera brumata. Oecologia 136:244–251CrossRefGoogle Scholar
  82. Torres-Vila LM, Rodríguez-Molina MC, McMinn M, Rodríguez-Molina A (2004) Larval food source promotes cyclic seasonal variation in polyandry in the moth Lobesia botrana. Behav Ecol 16:114–122CrossRefGoogle Scholar
  83. Twiss E, Coros AM, Tavakoli NP, Derbyshire KM (2005) Transposition is modulated by a diverse set of host factors in Escherechia coli and is stimulated by nutritional stress. Mol Microbiol 57:1593–1607CrossRefGoogle Scholar
  84. Valiela I (1995) Marine ecological processes, 2nd edn. Springer, New YorkGoogle Scholar
  85. van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55CrossRefGoogle Scholar
  86. Varpe Ø, Fiksen Ø (2010) Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging. Ecology 91:311–318CrossRefGoogle Scholar
  87. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc Lond B 272:2561–2569CrossRefGoogle Scholar
  88. Visser ME, Holleman LJM (2000) Warmer springs disrupt the sunchrony of oak and winter moth phenology. Proc R Soc Lond B 268:289–294CrossRefGoogle Scholar
  89. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870CrossRefGoogle Scholar
  90. Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110CrossRefGoogle Scholar
  91. Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impacts on the breeding biology of an insectivorous bird. Oecologia 147:164–172CrossRefGoogle Scholar
  92. Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R, Fabian B, Heinrich W, Kohler G, Lichter D, Marstaller R, Sander FW (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453CrossRefGoogle Scholar
  93. Wassmann P, Duarte DM, Agusti S, Sejr MK (2010) Footprints of climate change in the Arctic marine ecosystem. Glob Change Biol 17:1235–1249CrossRefGoogle Scholar
  94. Winder M, Cloern JE (2010) The annual cycles of phytoplankton biomass. Philos Trans R Soc Lond B 365:3215–3226CrossRefGoogle Scholar
  95. Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106CrossRefGoogle Scholar

Copyright information

© ISB 2011

Authors and Affiliations

  • Alison Donnelly
    • 1
    Email author
  • Amelia Caffarra
    • 1
    • 2
  • Bridget F. O’Neill
    • 1
  1. 1.Centre for the Environment, School of Natural SciencesTrinity College DublinDublinIreland
  2. 2.Sustainable Agroecosystems and Bioresources, Research and Innovation CentreFondazione Edmund Mach, Instituto AgrarioTrentoItaly

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