Becoming nose-blind-Climate change impacts on chemical communication.

behavior; chemoreception; climate change stressor; ecological interactions; infochemicals; ocean acidification; semiochemicals; sensory ecology; General Environmental Science; Ecology; Environmental Chemistry; Global and Planetary Change

Abstract :

[en] Chemical communication via infochemicals plays a pivotal role in ecological interactions, allowing organisms to sense their environment, locate predators, food, habitats, or mates. A growing number of studies suggest that climate change-associated stressors can modify these chemically mediated interactions, causing info-disruption that scales up to the ecosystem level. However, our understanding of the underlying mechanisms is scarce. Evidenced by a range of examples, we illustrate in this opinion piece that climate change affects different realms in similar patterns, from molecular to ecosystem-wide levels. We assess the importance of different stressors for terrestrial, freshwater, and marine ecosystems and propose a systematic approach to address highlighted knowledge gaps and cross-disciplinary research avenues.

Disciplines :

Aquatic sciences & oceanology
Zoology
Animal psychology, ethology & psychobiology

Author, co-author :

Roggatz, Christina C ; Energy and Environment Institute, University of Hull, Hull, UK

Saha, Mahasweta ; Plymouth Marine Laboratory, Plymouth, UK

Blanchard, Solène ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Schirrmacher, Paula ; Department of Biological and Marine Sciences, University of Hull, Hull, UK

Fink, Patrick ; Department River Ecology, Helmholtz Centre for Environmental Research GmbH - UFZ, Magdeburg, Germany ; Department Aquatic Ecosystem Analysis and Management, Helmholtz Centre for Environmental Research GmbH - UFZ, Magdeburg, Germany

Verheggen, François ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Hardege, Jörg D ; Department of Biological and Marine Sciences, University of Hull, Hull, UK

Language :

English

Title :

Becoming nose-blind-Climate change impacts on chemical communication.

Publication date :

16 May 2022

Journal title :

Global Change Biology

ISSN :

1354-1013

eISSN :

1365-2486

Publisher :

Wiley, England

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://onlinelibrary.wiley.com/doi/pdf/10.1111/gcb.16209

Funders :

DFG - Deutsche Forschungsgemeinschaft [DE]
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
ERC - European Research Council [BE]
Natural Environment Research Council
University of Hull

Available on ORBi :

since 17 June 2022

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Bibliography

Abboud, J.-C., Bartolome, E. A., Blanco, M., Kress, A. C., Ellis, I. Y., Yazzolino, P. K., Sorensen, K. I., Winslow, J. R., Cleary, D. A., & Lefcort, H. (2019). Carbon dioxide enrichment alters predator avoidance and sex determination but only sex is mediated by GABAA receptors. Hydrobiologia, 829(1), 307–322. https://doi.org/10.1007/s10750-018-3841-3
Allison, V., Dunham, D. W., & Harvey, H. H. (1992). Low pH alters response to food in the crayfish Cambarus bartoni. Canadian Journal of Zoology, 70(12), 2416–2420. https://doi.org/10.1139/z92-324
Baumann, H., & Smith, E. M. (2018). Quantifying metabolically driven pH and oxygen fluctuations in US nearshore habitats at diel to interannual time scales. Estuaries and Coasts, 41(4), 1102–1117. https://doi.org/10.1007/s12237-017-0321-3
Blanchard, S., Lognay, G., Verheggen, F., & Detrain, C. (2019). Today and tomorrow: Impact of climate change on aphid biology and potential consequences on their mutualism with ants: Aphid biology under climate change. Physiological Entomology, 44(2), 77–86. https://doi.org/10.1111/phen.12275
Blanchard, S., Van Offelen, J., Verheggen, F., & Detrain, C. (2021). Towards more intimacy: Moderate elevation of temperature drives increases in foraging and mutualistic interactions between Lasius Niger and Aphis fabae. Ecological Entomology, 46(2), 406–418. https://doi.org/10.1111/een.12982
Boullis, A., Blanchard, S., Francis, F., & Verheggen, F. (2018). Elevated CO2 concentrations impact the semiochemistry of aphid honeydew without having a cascade effect on an aphid predator. Insects, 9(2), 47. https://doi.org/10.3390/insects9020047
Boullis, A., Detrain, C., Francis, F., & Verheggen, F. J. (2016). Will climate change affect insect pheromonal communication? Current Opinion in Insect Science, 17, 87–91. https://doi.org/10.1016/j.cois.2016.08.006
Boullis, A., Fassotte, B., Sarles, L., Lognay, G., Heuskin, S., Vanderplanck, M., Bartram, S., Haubruge, E., Francis, F., & Verheggen, F. J. (2017). Elevated carbon dioxide concentration reduces alarm signaling in aphids. Journal of Chemical Ecology, 43(2), 164–171. https://doi.org/10.1007/s10886-017-0818-z
Boullis, A., Francis, F., & Verheggen, F. (2018). Aphid-hoverfly interactions under elevated CO2 concentrations: Oviposition and larval development. Physiological Entomology, 43(3), 245–250. https://doi.org/10.1111/phen.12253
Boullis, A., Francis, F., & Verheggen, F. J. (2015). Climate change and tritrophic interactions: Will modifications to greenhouse gas emissions increase the vulnerability of herbivorous insects to natural enemies? Environmental Entomology, 44(2), 277–286. https://doi.org/10.1093/ee/nvu019
Brady, R. X., Lovenduski, N. S., Yeager, S. G., Long, M. C., & Lindsay, K. (2020). Skillful multiyear predictions of ocean acidification in the California current system. Nature Communications, 11, 2166. https://doi.org/10.1038/s41467-020-15722-x
Brönmark, C., & Hansson, L.-A. (Eds.). (2012). Chemical ecology in aquatic systems—An introduction. In Chemical ecology in aquatic systems (pp. xiv–xix). Oxford University Press.
Brown, G. E., Adrian, J. C., Jr., Lewis, M. G., & Tower, J. M. (2002). The effects of reduced pH on chemical alarm signalling in ostariophysan fishes. Canadian Journal of Fisheries and Aquatic Sciences, 59(8), 1331–1338. https://doi.org/10.1139/f02-104
Brown, G. E., Elvidge, C. K., Ferrari, M. C. O., & Chivers, D. P. (2012). Understanding the importance of episodic acidification on fish predator–prey interactions: Does weak acidification impair predator recognition? Science of the Total Environment, 439, 62–66. https://doi.org/10.1016/j.scitotenv.2012.09.026
Burks, R. L., & Lodge, D. M. (2002). Cued in: Advances and opportunities in freshwater chemical ecology. Journal of Chemical Ecology, 28, 1901–1917. https://doi.org/10.1023/A:1020785525081
Buxton, V. L., Enos, J. K., Sperry, J. H., & Ward, M. P. (2020). A review of conspecific attraction for habitat selection across taxa. Ecology and Evolution, 10(23), 12690–12699. https://doi.org/10.1002/ece3.6922
Calosi, P., Rastrick, S. P. S., Lombardi, C., de Guzman, H. J., Davidson, L., Jahnke, M., Giangrande, A., Hardege, J. D., Schulze, A., Spicer, J. I., & Gambi, M.-C. (2013). Adaptation and acclimatization to ocean acidification in marine ectotherms: An in situ transplant experiment with polychaetes at a shallow CO2 vent system. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1627), 20120444. https://doi.org/10.1098/rstb.2012.0444
Campbell, A. H., Harder, T., Nielsen, S., Kjelleberg, S., & Steinberg, P. D. (2011). Climate change and disease: Bleaching of a chemically defended seaweed. Global Change Biology, 17(9), 2958–2970. https://doi.org/10.1111/j.1365-2486.2011.02456.x
Charpentier, C. L., & Cohen, J. H. (2016). Acidification and γ -aminobutyric acid independently alter kairomone-induced behaviour. Royal Society Open Science, 3(9), 160311. https://doi.org/10.1098/rsos.160311
Chen, Y., Serteyn, L., Wang, Z., He, K., & Francis, F. (2019). Reduction of plant suitability for corn leaf aphid (Hemiptera: Aphididae) under elevated carbon dioxide condition. Environmental Entomology, 48(4), 10–944. https://doi.org/10.1093/ee/nvz045
Chivers, D. P., McCormick, M. I., Nilsson, G. E., Munday, P. L., Watson, S.-A., Meekan, M. G., Mitchell, M. D., Corkill, K. C., & Ferrari, M. C. O. (2014). Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference. Global Change Biology, 20(2), 515–522. https://doi.org/10.1111/gcb.12291
Clark, T. D., Raby, G. D., Roche, D. G., Binning, S. A., Speers-Roesch, B., Jutfelt, F., & Sundin, J. (2020a). Ocean acidification does not impair the behaviour of coral reef fishes. Nature, 577(7790), 370–375. https://doi.org/10.1038/s41586-019-1903-y
Clark, T. D., Raby, G. D., Roche, D. G., Binning, S. A., Speers-Roesch, B., Jutfelt, F., & Sundin, J. (2020b). Reply to: Methods matter in repeating ocean acidification studies. Nature, 586(7830), E25–E27. https://doi.org/10.1038/s41586-020-2804-9
Clements, J., & Hunt, H. (2015). Marine animal behaviour in a high CO2 ocean. Marine Ecology Progress Series, 536, 259–279. https://doi.org/10.3354/meps11426
Clements, J., Sundin, J., Clark, T. D., & Jutfelt, F. (2022). Meta-analysis reveals an extreme “decline effect” in the impacts of ocean acidification on fish behavior. PLoS Biology, 20(2), e3001511. https://doi.org/10.1371/journal.pbio.3001511
Da Gama, B. A. P., Pereira, R. C., Soares, A. R., Teixeira, V. L., & Yoneshigue-Valentin, Y. (2003). Is the mussel test a good indicator of antifouling activity? A comparison between laboratory and field assays. Biofouling, 19(1), 161–169. https://doi.org/10.1080/0892701031000089534
de la Haye, K. L., Spicer, J. I., Widdicombe, S., & Briffa, M. (2012). Reduced pH sea water disrupts chemo-responsive behaviour in an intertidal crustacean. Journal of Experimental Marine Biology and Ecology, 412, 134–140. https://doi.org/10.1016/j.jembe.2011.11.013
Draper, A. M., & Weissburg, M. J. (2019). Impacts of global warming and elevated CO2 on sensory behavior in predator-prey interactions: A review and synthesis. Frontiers in Ecology and Evolution, 7, 72. https://doi.org/10.3389/fevo.2019.00072
Engel, A., Zondervan, I., Aerts, K., Beaufort, L., Benthien, A., Chou, L., Delille, B., Gattuso, J.-P., Harlay, J., Heemann, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M.-D., Rochelle-Newall, E., Schneider, U., Terbrueggen, A., & Riebesell, U. (2005). Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnology and Oceanography, 50(2), 493–507. https://doi.org/10.4319/lo.2005.50.2.0493
Ferrari, M. C. O., Wisenden, B. D., & Chivers, D. P. (2010). Chemical ecology of predator–prey interactions in aquatic ecosystems: A review and prospectus. Canadian Journal of Zoology, 88(7), 698–724. https://doi.org/10.1139/Z10-029
Fink, P., Norf, H., Anlanger, C., Brauns, M., Kamjunke, N., Risse-Buhl, U., Schmitt-Jansen, M., Weitere, M., & Borchardt, D. (2020). Streamside mobile mesocosms (MOBICOS): A new modular research infrastructure for hydro-ecological process studies across catchment-scale gradients. International Review of Hydrobiology, 105(3–4), 63–73. https://doi.org/10.1002/iroh.201902009
Foo, S. A., Byrne, M., & Gambi, M. C. (2018). The carbon dioxide vents of Ischia, Italy, a natural system to assess impacts of ocean acidification on marine ecosystems. Oceanography and Marine Biology: An Annual Review, 56, 237–310.
Furlong, M. J., & Zalucki, M. P. (2017). Climate change and biological control: The consequences of increasing temperatures on host–parasitoid interactions. Current Opinion in Insect Science, 20, 39–44. https://doi.org/10.1016/j.cois.2017.03.006
Griffiths, R. A. (1993). The effect of pH on feeding behaviour in newt larvae (Triturus: Amphibia). Journal of Zoology, 231(2), 285–290. https://doi.org/10.1111/j.1469-7998.1993.tb01918.x
Groot, A. T., & Zizzari, Z. V. (2019). Does climate warming influence sexual chemical signaling? Animal Biology, 69(1), 83–93. https://doi.org/10.1163/15707563-20191103
Guan, C., Saha, M., & Weinberger, F. (2020). Simulated heatwaves lead to upregulated chemical defence of a marine foundation macrophyte against microbial colonisers. Frontiers in Marince Science, 7, 463. https://doi.org/10.3389/fmars.2020.00463
Hanazato, T. (1991). Effects of a Chaoborus-released chemical on Daphnia ambigua: Reduction in the tolerance of the Daphnia to summer water temperature. Limnology and Oceanography, 36(1), 165–171. https://doi.org/10.4319/lo.1991.36.1.0165
Hasler, C. T., Jeffrey, J. D., Schneider, E. V. C., Hannan, K. D., Tix, J. A., & Suski, C. D. (2018). Biological consequences of weak acidification caused by elevated carbon dioxide in freshwater ecosystems. Hydrobiologia, 806(1), 1–12. https://doi.org/10.1007/s10750-017-3332-y
Hay, M. E. (2009). Marine chemical ecology: Chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science, 1, 193–212.
Hentley, W. T., Vanbergen, A. J., Hails, R. S., Jones, T. H., & Johnson, S. N. (2014). Elevated atmospheric CO2 impairs aphid escape responses to predators and conspecific alarm signals. Journal of Chemical Ecology, 40(10), 1110–1114. https://doi.org/10.1007/s10886-014-0506-1
Hentley, W. T., & Wade, R. N. (2016). Global change, herbivores and their natural enemies. In S. N. Johnson & T. H. Jones (Eds.), Global climate change and terrestrial invertebrates (pp. 177–200). John Wiley & Sons Ltd. https://doi.org/10.1002/9781119070894.ch10
Ianora, A., Miralto, A., Poulet, S. A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T., Colucci-D'Amato, L., Terrazzano, G., & Smetacek, V. (2004). Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature, 429(6990), 403–407. https://doi.org/10.1038/nature02526
IPCC. (2021). Climate change 2021: The physical science basis. In V. Masson-Delmotte, P. Zhai, A. Pirani, S. L. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M. I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J. B. R. Matthews, T. K. Maycock, T. Waterfield, O. Yelekçi, R. Yu, & B. Zhou (Eds.), Contribution of working group I to the sixth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press.
Jactel, H., Brockerhoff, E., & Duelli, P. (2005). A test of the biodiversity-stability theory: Meta-analysis of tree species diversity effects on insect pest infestations, and re-examination of responsible factors. In M. Scherer-Lorenzen, C. Körner, & E.-D. Schulze (Eds.), Forest diversity and function (Vol. 176, pp. 235–262). Springer-Verlag. https://doi.org/10.1007/3-540-26599-6_12
Kamio, M., & Derby, C. D. (2017). Finding food: How marine invertebrates use chemical cues to track and select food. Natural Product Reports, 34(5), 514–528. https://doi.org/10.1039/C6NP00121A
Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F., & Bronstein, J. L. (2010). Mutualisms in a changing world: An evolutionary perspective. Ecology Letters, 13(12), 1459–1474. https://doi.org/10.1111/j.1461-0248.2010.01538.x
Kozma, M. T., Schmidt, M., Ngo-Vu, H., Sparks, S. D., Senatore, A., & Derby, C. D. (2018). Chemoreceptor proteins in the Caribbean spiny lobster, Panulirus argus: Expression of ionotropic receptors, gustatory receptors, and trp channels in two chemosensory organs and brain. PLoS One, 13(9), e0203935. https://doi.org/10.1371/journal.pone.0203935
Leal, W. S. (2013). Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58(1), 373–391. https://doi.org/10.1146/annurev-ento-120811-153635
Leduc, A. O. H. C., Munday, P. L., Brown, G. E., & Ferrari, M. C. O. (2013). Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: A synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1627), 20120447. https://doi.org/10.1098/rstb.2012.0447
Lucey, N. M., Lombardi, C., DeMarchi, L., Schulze, A., Gambi, M. C., & Calosi, P. (2015). To brood or not to brood: Are marine invertebrates that protect their offspring more resilient to ocean acidification? Scientific Reports, 5(1), 12009. https://doi.org/10.1038/srep12009
Maibam, C., Fink, P., Romano, G., Buia, M. C., Butera, E., & Zupo, V. (2015). Centropages typicus (Crustacea, Copepoda) reacts to volatile compounds produced by planktonic algae. Marine Ecology, 36(3), 819–834. https://doi.org/10.1111/maec.12254
Maibam, C., Fink, P., Romano, G., Buia, M. C., Gambi, M. C., Scipione, M. B., Patti, F. P., Lorenti, M., Butera, E., & Zupo, V. (2014). Relevance of wound-activated compounds produced by diatoms as toxins and infochemicals for benthic invertebrates. Marine Biology, 161(7), 1639–1652. https://doi.org/10.1007/s00227-014-2448-0
Manefield, M., Rasmussen, T. B., Henzter, M., Andersen, J. B., Steinberg, P., Kjelleberg, S., & Givskov, M. (2002). Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology, 148(4), 1119–1127. https://doi.org/10.1099/00221287-148-4-1119
Mondor, E. B., Tremblay, M. N., Awmack, C. S., & Lindroth, R. L. (2004). Divergent pheromone-mediated insect behaviour under global atmospheric change. Global Change Biology, 10(10), 1820–1824. https://doi.org/10.1111/j.1365-2486.2004.00838.x
Mondor, E. B., Tremblay, M. N., Awmack, C. S., & Lindroth, R. L. (2005). Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres. Global Change Biology, 11, 1990–1996. https://doi.org/10.1111/j.1365-2486.2005.1054.x
Munday, P. L., Dixson, D. L., Welch, M. J., Chivers, D. P., Domenici, P., Grosell, M., Heuer, R. M., Jones, G. P., McCormick, M. I., Meekan, M., Nilsson, G. E., Ravasi, T., & Watson, S.-A. (2020). Methods matter in repeating ocean acidification studies. Nature, 586(7830), E20–E24. https://doi.org/10.1038/s41586-020-2803-x
Mutalipassi, M., Fink, P., Maibam, C., Porzio, L., Buia, M. C., Gambi, M. C., Patti, F. P., Scipione, M. B., Lorenti, M., & Zupo, V. (2020). Ocean acidification alters the responses of invertebrates to wound-activated infochemicals produced by epiphytes of the seagrass Posidonia oceanica. Journal of Experimental Marine Biology and Ecology, 530–531, 151435. https://doi.org/10.1016/j.jembe.2020.151435
Mutalipassi, M., Mazzella, V., Schott, M., Fink, P., Glaviano, F., Porzio, L., Lorenti, M., Buia, M. C., von Elert, E., & Zupo, V. (2022). Ocean acidification affects volatile infochemicals production and perception in fauna and flora associated with Posidonia oceanica (L.) Delile. Frontiers in Marine Science, 9, 809702. https://doi.org/10.3389/fmars.2022.809702
Nilsson, G. E., Dixson, D. L., Domenici, P., McCormick, M. I., Sørensen, C., Watson, S.-A., & Munday, P. L. (2012). Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change, 2(3), 201–204. https://doi.org/10.1038/nclimate1352
Ou, M., Hamilton, T. J., Eom, J., Lyall, E. M., Gallup, J., Jiang, A., Lee, J., Close, D. A., Yun, S.-S., & Brauner, C. J. (2015). Responses of pink salmon to CO2-induced aquatic acidification. Nature Climate Change, 5(10), 950–955. https://doi.org/10.1038/nclimate2694
Parachnowitsch, A. L., & Manson, J. S. (2015). The chemical ecology of plant-pollinator interactions: Recent advances and future directions. Current Opinion in Insect Science, 8, 41–46. https://doi.org/10.1016/j.cois.2015.02.005
Pereira, R. C., da Gama, B. A. P., Teixeira, V. L., & Yoneshigue-Valentin, Y. (2003). Ecological roles of natural products of the Brazilian red seaweed Laurencia obtusa. Brazilian Journal of Biology, 63(4), 665–672. https://doi.org/10.1590/S1519-69842003000400013
Porteus, C. S., Hubbard, P. C., Uren Webster, T. M., van Aerle, R., Canário, A. V. M., Santos, E. M., & Wilson, R. W. (2018). Near-future CO2 levels impair the olfactory system of a marine fish. Nature Climate Change, 8(8), 737–743. https://doi.org/10.1038/s41558-018-0224-8
Rittschof, D., & Cohen, J. H. (2004). Crustacean peptide and peptide-like pheromones and kairomones. Peptides, 25(9), 1503–1516. https://doi.org/10.1016/j.peptides.2003.10.024
Roggatz, C. C., Fletcher, N., Benoit, D. M., Algar, A. C., Doroff, A., Wright, B., Wollenberg Valero, K. C., & Hardege, J. D. (2019). Saxitoxin and tetrodotoxin bioavailability increases in future oceans. Nature Climate Change, 9, 840–844. https://doi.org/10.1038/s41558-019-0589-3
Roggatz, C. C., Kenningham, N., & Bartels-Hardege, H. D. (2019). Taking current climate change research to the classroom—The “Will hermit crabs go hungry in future oceans?” project. In W. Leal Filho & S. L. Hemstock (Eds.), Climate change and the role of education (pp. 255–277). Springer International Publishing. https://doi.org/10.1007/978-3-030-32898-6_15
Roggatz, C. C., Lorch, M., Hardege, J. D., & Benoit, D. M. (2016). Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules. Global Change Biology, 22(12), 3914–3926. https://doi.org/10.1111/gcb.13354
Saha, M., Barboza, F. R., Somerfield, P. J., Al-Janabi, B., Beck, M., Brakel, J., Ito, M., Pansch, C., Nascimento-Schulze, J. C., Jakobsson Thor, S., Weinberger, F., & Sawall, Y. (2020). Response of foundation macrophytes to near-natural simulated marine heatwaves. Global Change Biology, 26(2), 417–430. https://doi.org/10.1111/gcb.14801
Saha, M., Berdalet, E., Carotenuto, Y., Fink, P., Harder, T., John, U., Not, F., Pohnert, G., Potin, P., Selander, E., Vyverman, W., Wichard, T., Zupo, V., & Steinke, M. (2019). Using chemical language to shape future marine health. Frontiers in Ecology and the Environment, 17(9), 530–537. https://doi.org/10.1002/fee.2113
Saha, M., Goecke, F., & Bhadury, P. (2018). Minireview: Algal natural compounds and extracts as antifoulants. Journal of Applied Phycology, 30(3), 1859–1874. https://doi.org/10.1007/s10811-017-1322-0
Saha, M., & Weinberger, F. (2019). Microbial “gardening” by a seaweed holobiont: Surface metabolites attract protective and deter pathogenic epibacterial settlement. Journal of Ecology, 107(5), 2265. https://doi.org/10.1111/1365-2745.13193
Schindler, D. W. (1988). Effects of acid rain on freshwater ecosystems. Science, 239(4836), 149–157. https://doi.org/10.1126/science.239.4836.149
Schirrmacher, P., Roggatz, C. C., Benoit, D. M., & Hardege, J. D. (2021). Ocean acidification amplifies the olfactory response to 2-phenylethylamine: Altered cue reception as a mechanistic pathway? Journal of Chemical Ecology, 47, 859–876. https://doi.org/10.1007/s10886-021-01276-9
Senior, V. L., Evans, L. C., Leather, S. R., Oliver, T. H., & Evans, K. L. (2020). Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study. Global Change Biology, 26(5), 2814–2828. https://doi.org/10.1111/gcb.15015
Sentis, A., Ramon-Portugal, F., Brodeur, J., & Hemptinne, J.-L. (2015). The smell of change: Warming affects species interactions mediated by chemical information. Global Change Biology, 21(10), 3586–3594. https://doi.org/10.1111/gcb.12932
Sudatti, D. B., Fujii, M. T., Rodrigues, S. V., Turra, A., & Pereira, R. C. (2011). Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Marine Biology, 158(7), 1439–1446. https://doi.org/10.1007/s00227-011-1660-4
Sun, Y., Su, J., & Ge, F. (2010). Elevated CO2 reduces the response of Sitobion avenae (Homoptera: Aphididae) to alarm pheromone. Agriculture, Ecosystems & Environment, 135(1–2), 140–147. https://doi.org/10.1016/j.agee.2009.09.011
Sunday, J. M., Calosi, P., Dupont, S., Munday, P. L., Stillman, J. H., & Reusch, T. B. H. (2014). Evolution in an acidifying ocean. Trends in Ecology & Evolution, 29(2), 117–125. https://doi.org/10.1016/j.tree.2013.11.001
Tembo, R. N. (2009). The sublethal effects of low-pH exposure on the chemoreception of Poecilia sphenops. Archives of Environmental Contamination and Toxicology, 57(1), 157–163. https://doi.org/10.1007/s00244-008-9255-x
Tierney, A. J., & Atema, J. (1986). Effects of acidification on the behavioral response of crayfishes (Orconectes virilis and Procambarus acutus) to chemical stimuli. Aquatic Toxicology, 9(1), 1–11. https://doi.org/10.1016/0166-445X(86)90002-0
Tix, J. A., Hasler, C. T., Sullivan, C., Jeffrey, J. D., & Suski, C. D. (2017). Elevated carbon dioxide has the potential to impact alarm cue responses in some freshwater fishes. Aquatic Ecology, 51(1), 59–72. https://doi.org/10.1007/s10452-016-9598-8
Toth, G. B., & Pavia, H. (2000). Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). Proceedings of the National Academy of Sciences, 97(26), 14418–14420. https://doi.org/10.1073/pnas.250226997
Ulseth, A. J., Bertuzzo, E., Singer, G. A., Schelker, J., & Battin, T. J. (2018). Climate-induced changes in spring snowmelt impact ecosystem metabolism and carbon fluxes in an alpine stream network. Ecosystems, 21(2), 373–390. https://doi.org/10.1007/s10021-017-0155-7
van Oudenhove, L., Billoir, E., Boulay, R., Bernstein, C., & Cerdá, X. (2011). Temperature limits trail following behaviour through pheromone decay in ants. Naturwissenschaften, 98(12), 1009–1017. https://doi.org/10.1007/s00114-011-0852-6
Vanderplanck, M., Lapeyre, B., Brondani, M., Opsommer, M., Dufay, M., Hossaert-McKey, M., & Proffit, M. (2021). Ozone pollution alters olfaction and behavior of pollinators. Antioxidants, 10(5), 636. https://doi.org/10.3390/antiox10050636
Velez, Z., Roggatz, C. C., Benoit, D. M., Hardege, J. D., & Hubbard, P. C. (2019). Short- and medium-term exposure to ocean acidification reduces olfactory sensitivity in gilthead seabream. Frontiers in Physiology, 10, 731. https://doi.org/10.3389/fphys.2019.00731
Verheggen, F. J., Arnaud, L., Bartram, S., Gohy, M., & Haubruge, E. (2008). Aphid and plant volatiles induce oviposition in an Aphidophagous hoverfly. Journal of Chemical Ecology, 34(3), 301–307. https://doi.org/10.1007/s10886-008-9434-2
Verheggen, F. J., Diez, L., Sablon, L., Fischer, C., Bartram, S., Haubruge, E., & Detrain, C. (2012). Aphid alarm pheromone as a cue for ants to locate aphid partners. PLoS One, 7(8), e41841. https://doi.org/10.1371/journal.pone.0041841
Wäge, J., Valvassori, G., Hardege, J. D., Schulze, A., & Gambi, M. C. (2017). The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: Are phylogeographic patterns related to exposure to ocean acidification? Marine Biology, 164, 199. https://doi.org/10.1007/s00227-017-3222-x
Weiss, L. C., Albada, B., Becker, S. M., Meckelmann, S. W., Klein, J., Meyer, M., Schmitz, O. J., Sommer, U., Leo, M., Zagermann, J., Metzler-Nolte, N., & Tollrian, R. (2018). Identification of Chaoborus kairomone chemicals that induce defences in Daphnia. Nature Chemical Biology, 14(12), 1133–1139. https://doi.org/10.1038/s41589-018-0164-7
Weiss, L. C., Pötter, L., Steiger, A., Kruppert, S., Frost, U., & Tollrian, R. (2018). Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia. Current Biology, 28(2), 327–332.e3. https://doi.org/10.1016/j.cub.2017.12.022
Wetzel, R. G. (2011). Limnology: Lake and river ecosystems (3rd ed.). Academic Press.
Wisenden, B. D. (2000). Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1401), 1205–1208. https://doi.org/10.1098/rstb.2000.0668
Wolfe, K., Nguyen, H. D., Davey, M., & Byrne, M. (2020). Characterizing biogeochemical fluctuations in a world of extremes: A synthesis for temperate intertidal habitats in the face of global change. Global Change Biology, 26(7), 3858–3879. https://doi.org/10.1111/gcb.15103
Wyatt, T. D. (2003). Pheromones and animal behaviour: Communication by smell and taste. Cambridge University Press.
Wyatt, T. D. (2014). Pheromones and animal behaviour: Chemical signals and signatures (2nd ed.). Cambridge University Press.
Zupo, V., Maibam, C., Buia, M. C., Gambi, M. C., Patti, F. P., Scipione, M. B., Lorenti, M., & Fink, P. (2015). Chemoreception of the seagrass Posidonia oceanica by benthic invertebrates is altered by seawater acidification. Journal of Chemical Ecology, 41(8), 766–779. https://doi.org/10.1007/s10886-015-0610-x
Zupo, V., Mutalipassi, M., Fink, P., & Di Natale, M. (2016). Effect of ocean acidification on the communications among invertebrates mediated by plant-produced volatile organic compounds. Global Journal of Ecology, 1(1), 12–18. https://doi.org/10.17352/gje.000002