Abstract
Several plants and invertebrates interact and communicate by means of volatile organic compounds (VOCs). These compounds may play the role of infochemicals, being able to carry complex information to selected species, thus mediating inter- or intra-specific communications. Volatile organic compounds derived from the wounding of marine diatoms, for example, carry information for several benthic and planktonic invertebrates. Although the ecological importance of VOCs has been demonstrated, both in terrestrial plants and in marine microalgae, their role as infochemicals has not been demonstrated in seagrasses. In addition, benthic communities, even the most complex and resilient, as those associated to seagrass meadows, are affected by ocean acidification at various levels. Therefore, the acidification of oceans could produce interference in the way seagrass-associated invertebrates recognize and choose their specific environments. We simulated the wounding of Posidonia oceanica leaves collected at two sites (a control site at normal pH, and a naturally acidified site) off the Island of Ischia (Gulf of Naples, Italy). We extracted the VOCs and tested a set of 13 species of associated invertebrates for their specific chemotactic responses in order to determine if: a) seagrasses produce VOCs playing the role of infochemicals, and b) their effects can be altered by seawater pH. Our results indicate that several invertebrates recognize the odor of wounded P. oceanica leaves, especially those strictly associated to the leaf stratum of the seagrass. Their chemotactic reactions may be modulated by the seawater pH, thus impairing the chemical communications in seagrass-associated communities in acidified conditions. In fact, 54 % of the tested species exhibited a changed behavioral response in acidified waters (pH 7.7). Furthermore, the differences observed in the abundance of invertebrates, in natural vs. acidified field conditions, are in agreement with these behavioral changes. Therefore, leaf-produced infochemicals may influence the structure of P. oceanica epifaunal communities, and their effects can be regulated by seawater acidification.
Similar content being viewed by others
References
Apostolaki ET, Vizzini S, Hendriks IE, Olsen YS (2014) Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent. Mar Environ Res 99:9–15. doi:10.1016/j.marenvres.2014.05.008
Arnold T, Mealey C, Leahey H, Miller AW, Hall-Spencer JM, Milazzo M, Maers K (2012) Ocean acidification and the loss of phenolic substances in marine plants. Plos One 7, e35107. doi:10.1371/journal.pone.0035107
Brewer PG (2013) A short history of ocean acidification science in the 20th century: a chemist’s view. Biogeosciences 10:7411–7422. doi:10.5194/bg-10-7411-2013
Briffa M, de la Haye K, Munday PL (2012) High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar Pollut Bull 64:1519–1528. doi:10.1016/j.marpolbul.2012.05.032
Buia MC, Zupo V, Mazzella L (1992) Primary production and growth dynamics in Posidonia oceanica. PSZN I: Mar Ecol 13:2–16. doi:10.1111/j.1439-0485.1992.tb00336.x
Buia MC, Gambi MC, Dappiano M (2004) The seagrass systems. In: Gambi MC, Dappiano M (eds) Mediterranean marine benthos: a manual of methods for its sampling and study. Biol Mar Mediterr 11 (Suppl. 1), Chap. 5, pp 133–184
Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res Oceans 110:C9. doi:10.1029/2004JC002671
Campbell JE, Fourqurean JW (2013) Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum. Mar Biol 160:1465–1475. doi:10.1007/s00227-013-2199-3
Chase R (1982) The olfactory sensitivity of snails, Achatina fulica. J Comp Physiol 148:225–235. doi:10.1007/BF00619129
Cigliano M, Gambi MC, Rodolfo-Metalpa R, Patti FP, Hall-Spencer JM (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502. doi:10.1007/s00227-010-1513-6
Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than original compounds? Funct Ecol 2:131–139
Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75. doi:10.1111/j.1461-0248.2009.01400.x
Dolecal RE, Long JD (2014) Chemically mediated foraging by subtidal marine predators: a field test of tritrophic cues. Mar Ecol Prog Ser 498:161–169. doi:10.3354/meps10627
Donnarumma L, Lombardi C, Cocito S, Gambi MC (2014) Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Med Mar Sci. doi:10.12681/mms.677
Fabricius KE, Déath G, Noonan S, Uthicke S (2014) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc R Soc B Biol Sci 281:1775. doi:10.1098/rspb.2013.2479
Fink P (2007) Ecological functions of volatile organic compounds in aquatic systems. Mar Freshw Behav Physiol 40:155–168. doi:10.1080/10236240701602218
Fink P, von Elert E, Jüttner F (2006a) Volatile foraging kairomones in the littoral zone: attraction of an herbivorous freshwater gastropod to algal odors. J Chem Ecol 32:1867–1881. doi:10.1007/s10886-006-9115-y
Fink P, von Elert E, Jüttner F (2006b) Oxylipins from freshwater diatoms act as attractants for a benthic herbivore. Arch Hydrobiol 167:561–574. doi:10.1127/0003-9136/2006/0167-0561
Gambi MC, Lorenti M, Russo GF, Scipione MB, Zupo V (1992) Depth and seasonal distribution of some groups of the vagile fauna of Posidonia oceanica leaf stratum: structural and feeding guild analyses. Mar Ecol 13:17–39. doi:10.1111/j.1439-0485.1992.tb00337.x
Garrard SL, Beaumont NJ (2014) The effect of ocean acidification on carbon storage and sequestration in seagrass beds; a global and UK context. Mar Pollut Bull 86:138–46. doi:10.1016/j.marpolbul.2014.07.032
Garrard SL, Hunter RC, Frommel AY, Lane AC, Phillips JC, Cooper R, Dineshram R, Cardini U, McCoy SJ, Arnberg M, Rodrigues Alves BG, Annane S, de Orte MR, Kumar A, Aguirre-Martinez GV, Maneja HH, Basallote MD, Ape F, Torstensson A, Bjoerk MM (2013) Biological impacts of ocean acidification: a postgraduate perspective on research priorities. Mar Biol 160:1789–1805. doi:10.1007/s00227-012-2033-3
Garrard SL, Gambi MC, Scipione MB, Patti FP, Lorenti M, Zupo V, Paterson DM, Buia MC (2014) Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. J Exp Mar Biol Ecol 421:31–38. doi:10.1016/jembe.2014.07.011
Gartner A, Tuya F, Lavery PS, McMahon K (2013) Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. J Exp Mar Biol Ecol 439:143–151. doi:10.1016/j.jembe.2012.11.009
Grote R., Monson RK, Niinemets Ü (2013) Leaf-level models of constitutive and stress-driven volatile organic compound emissions In: Niinemets Ü, Monson RK (eds.) Biology, controls and models of tree volatile organic compound emissions. Berlin: Springer Science + Business Media B.V. pp 315–355
Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99. doi:10.1038/nature07051
Horner AJ, Nickles SP, Weissburg MJ, Derby CD (2006) Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus). Biol Bull 211:28–139
Horner AJ, Schmidt M, Edwards DH, Derby CD (2008) Role of the olfactory pathway in agonistic behavior of crayfish Procambarus clarkii. Invertebr Neurosci 8:11–18. doi:10.1007/s10158-007-0063-1
IPCC (2007) Climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds.) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the inter-governmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA
James NC, Cowley PD, Whitfiels AK, Kaiser H (2008) Choice chamber experiments to test the attraction of postflexion Rhabdosargus holubi larvae to water of estuarine and riverine origin. Estuar Coast Shelf Sci 77:143–149. doi:10.1016/j.ecss.2007.09.010
Jernakoff P, Nielsen J (1998) Plant-animal associations in two species of seagrasses in Western Australia. Aquat Bot 60:359–376. doi:10.1016/S0304-3770(97)00100-9
Jüttner F (1988) Quantitative analysis of volatile organic-compounds. Methods Enzymol 167:609–616
Jüttner F, Messina P, Patalano C, Zupo V (2010) Odour compounds of the diatom Cocconeis scutellum: effects on benthic herbivores living on Posidonia oceanica. Mar Ecol Prog Ser 400:63–73. doi:10.3354/meps08381
Kaasik M, Sofiev M, Prank M, Ruuskanen T, Kukkonen J, Horrak U, Kulmala M (2011) Geographical origin of aerosol particles observed during the LAPBIAT measurement campaign in spring 2003 in Finnish Lapland. Boreal Environ Res 16:15–35
Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011) Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc Natl Acad Sci U S A 108:14515–14520. doi:10.1073/pnas.1107789108
Lebreton B, Richard P, Radenac G, Bordes M, Breret M, Arnaud C, Mornet F, Blanchard GF (2009) Are epiphytes a significant component of intertidal Zostera noltii beds? Aquat Bot 91:82–90. doi:10.1016/j.aquabot.2009.03.003
Lewis ND, Breckels MN, Archer SD, Morozov A, Pitchford SD, Steinke M, Codling EA (2012) Grazing-induced production of DMS can stabilize food-web dynamics and promote the formation of phytoplankton blooms in a multitrophic plankton model. Biogeochemistry 110:303–313. doi:10.1007/s10533-011-9649-0
Maibam C, Fink P, Romano G, Buia MC, Gambi MC, Scipione MB, Patti FP, Lorenti M, Butera E, Zupo V (2014) Relevance of wound-activated compounds produced by diatoms as toxins and infochemicals for benthic invertebrates. Mar Biol 161:1639–1652. doi:10.1007/s00227-014-2448-0
Maibam C, Fink P, Romano G, Buia MC, Butera E, Zupo V (2015) Centropages typicus (Crustacea, Copepoda) reacts to volatile compounds produced by planktonic algae. Mar Ecol. doi:10.1111/maec.12254
Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia MC, Gattuso JP, Hall-Spencer J (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4:689–692. doi:10.1098/rsbl.2008.0412
Matheron G (1969) Le krigeage universel. Les Cahiers Centre Morphologie Mathematique 1, Ecole des Mines de Paris
Matheron G (1970) La théorie des variables régionalisées et ses applications. Les Cahiers Centre Morphologie Mathematique, 5, Fontainebleau
Mazzella L, Buia MC, Gambi MC, Lorenti M, Russo GF, Scipione MB, Zupo V (1992) Plant-animal trophic relationships in the Posidonia oceanica ecosystem of the Mediterranean Sea: a review. In: Keegan JF (ed) Plant-animal interactions in marine benthos. London, pp 165–188
Monson RK, Grote R, Niinemets Ü, Schnitzler J-P (2012) Tansley review. Modeling the isoprene emission rate from leaves. New Phytol 195:541–559. doi:10.1111/j.1469- 8137.2012.04204.x
Niinemets Ü, Kännaste A, Copolovic L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:1–15. doi:10.3389/fpls.2013.00262
Pippen E, Nonaka M (1958) Notes - A convenient method for synthesizing normal aliphatic 2,4-dienals. J Org Chem 23:1580–1582
Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defense metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204. doi:10.1016/j.tree.2007.01.005
Ricevuto E, Lorenti M, Patti FP, Scipione MB, Gambi MC (2012) Temporal trends of benthic invertebrate settlement along a gradient of ocean acidification at natural CO2 vents (Tyrrhenian Sea). Biol Mar Mediterr 19:49–52
Ricevuto E, Kroeker KJ, Ferrigno F, Micheli F, Gambi MC (2014) Spatio-temporal variability of polychaete colonization at volcanic CO2 vents (Italy) indicates high tolerance to ocean acidification. Mar Biol. doi:10.1007/s00227-014-2555-y
Ricevuto E, Vizzini S, Gambi MC (2015) Ocean acidification effects on stable isotope signatures and trophic interactions of polychaete consumers and organic matter sources at a CO2 shallow vent system. J Exp Mar Biol Ecol 468:105–117. doi:10.1016/j.jembe.2015.03.016
Russo GF, Fraschetti S, Terlizzi A (2002) Population ecology and production of Bittium latreillii (Gastropoda, Cerithidae) in a Posidonia oceanica seagrass bed. Ital J Zool 69:215–222. doi:10.1080/11250000209356462
Scipione MB (2013) Do studies of functional groups give more insight to amphipod biodiversity? Crustaceana 86(7–8):955–1006. doi:10.1163/15685403-00003209
Sprinthall RC (2011) Basic Statistical Analysis. 9th Edition. Pearson Education Group
Steinke M, Malin G, Liss PS (2002) Trophic interactions in the sea: an ecological role for climate relevant volatiles? J Phycol 38:630–638. doi:10.1046/j.1529-8817.2002.02057.x
Tedesco D (1996) Chemical and isotopic investigations of fumarolic gases from Ischia island (southern Italy): evidences of magmatic and crustal contribution. J Volcanol Geotherm Res 74:233–242. doi:10.1016/S0377-0273(96)00030-3
Thoms C, Schupp PJ (2008) Activated chemical defense in marine sponges - a case study on Aplysinella rhax. J Chem Ecol 34:1242–1252. doi:10.1007/s10886-008-9518-z
Vos M, Vet LEM, Wackers FL, Middelburg JJ, van der Putten WH, Mooij WM, Heip CHR, van Donk E (2006) Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecol Inf 1:23–32. doi:10.1016/j.ecoinf.2005.06.001
Weissburg MJ, Zimmer-Faust RK (1991) Ontogeny versus phylogeny in determining patterns of chemoreception: initial studies with fiddler crabs. Biol Bull 181:205–215
Wichard T, Poulet SA, Halsband-Lenk C, Albaina A, Harris R, Liu D, Pohnert G (2005) Survey of the chemical defense potential of diatoms: screening of fifty one species for alpha, beta, gamma, delta-unsaturated aldehydes. J Chem Ecol 31:949–958. doi:10.1007/s10886-005-3615-z
Wyatt TD, Hardege JD, Terschak J (2014) Ocean acidification foils chemical signals. Science 346:176–176. doi:10.1126/science.346.6206.176-a
Zhou T, Rebach S (1999) Chemosensory orientation of the rock crab Cancer irroratus. J Chem Ecol 25:315–329. doi:10.1023/A:1020898830096
Zupo V, Nelson WG (1999) Factors influencing the association patterns of Hippolyte zostericola and Palaemonetes intermedius (Decapoda: Natantia) with seagrasses of the Indian River Lagoon, Florida. Mar Biol 134:181–190
Zupo V, Buia MC, Lorenti M, Procaccini G (2006) Temporal variations in the spatial distribution of shoot density in a Posidonia oceanica meadow and patterns of genetic diversity. PSZNI: Mar Ecol 27:328–338. doi:10.1111/j.1439-0485.2006.00133.x
Acknowledgments
This research was partially funded by the Flagship RITMARE - The Italian Research for the Sea - coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research. Chingoileima Maibam performed these studies in the frame of an Open University PhD course funded by SZN, under the supervision of V. Zupo. Patrick Fink was supported by an EU Assemble Marine Grant (No. 1060/G6). We are grateful to G. Romano (SZN) for help in the spectrophotometric evaluation of decadienal distribution. We thank Cpt. V. Rando for conducting the operations at sea on board the vessel Phoenicia of Stazione Zoologica Anton Dohrn.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zupo, V., Maibam, C., Buia, M.C. et al. Chemoreception of the Seagrass Posidonia Oceanica by Benthic Invertebrates is Altered by Seawater Acidification. J Chem Ecol 41, 766–779 (2015). https://doi.org/10.1007/s10886-015-0610-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-015-0610-x