Skip to main content
Log in

Relevance of wound-activated compounds produced by diatoms as toxins and infochemicals for benthic invertebrates

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Plants evolve the production of wound-activated compounds (WACs) to reduce grazing pressure. In addition, several plant-produced WACs are recognized by various invertebrates, playing the role of infochemicals. Due to co-evolutionary processes, some invertebrates recognize plant infochemicals and use them to identify possible prey, detect the presence of predators or identify algae containing various classes of toxic metabolites. Different metabolites present in the same algae can play the role of toxins, infochemicals or both simultaneously. We investigated the infochemical activity of compounds extracted from three diatoms epiphytes of the seagrass Posidonia oceanica, by conducting choice experiments on invertebrates living in the same community or in close proximity. Furthermore, the specific toxicity of the extracts obtained from the same algae was tested on sea urchin embryos using a standard bioassay procedure, to detect the presence of toxins. The comparison of the two effects demonstrated that invertebrates are subjected to diatom wound-activated toxicants when these algae are not associated with their own habitat, but they are able to recognize volatile infochemicals derived from diatoms associated with their habitats. The specific toxicity of WACs was shown to be inversely correlated to the perceptive ability of invertebrates towards volatile compounds liberated by the same algae. Hence, when the recognition of specific algae by a given invertebrate species evolves, their detrimental effects on the receiving organism may be lost.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • d’Ippolito G, Romano G, Caruso T, Spinella A, Cimino G, Fontana A (2003) Production of octadienal in the marine diatom Skeletonema costatum. Org Lett 5:885–887. doi:10.1021/ol034057c

    Article  Google Scholar 

  • De Stefano M, Marino D, Mazzella L (2000) Marine taxa of Cocconeis on leaves of Posidonia oceanica, including a new species and two new varieties. Eur J Phycol 35:225–242. doi:10.1080/09670260010001735831

    Article  Google Scholar 

  • Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than original compounds? Funct Ecol 2:131–139

    Article  Google Scholar 

  • Dutz J, Koski M, Jonasdottir SH (2008) Copepod reproduction is unaffected by diatom aldehydes or lipid composition. Limnol Oceanogr 53:225–235. doi:10.4319/lo.2008.53.1.0225

    Article  CAS  Google Scholar 

  • Fink P (2007) Ecological functions of volatile organic compounds in aquatic systems. Mar Freshw Behav Physiol 40:155–168. doi:10.1080/10236240701602218

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Flynn KJ, Irigoien X (2009) Aldehyde-induced insidious effects cannot be considered as a diatom defense mechanism against copepods. Mar Ecol Prog Ser 377:79–89. doi:10.3354/meps07865

    Article  Google Scholar 

  • Fontana A, d’Ippolito G, Cutignano A, Romano G, Lamari N, Gallucci AM, Cimino G, Miralto A, Ianora A (2007a) LOX-induced lipid peroxidation mechanism responsible for the detrimental effect of marine diatoms on zooplankton grazers. Chembiochem 8:1810–1818. doi:10.1002/cbic.200700269

    Article  CAS  Google Scholar 

  • Fontana A, d’Ippolito G, Cutignano A, Miralto A, Ianora A, Romano G, Cimino G (2007b) Oxylipin pathways in marine diatoms: a look at the chemical aspects. Pur Appl Chem 79:481–490. doi:10.1351/pac200779040481

    Article  CAS  Google Scholar 

  • Frontier S (1974) Contribution à la connaissance d’un écosistème néritique tropical: etude descriptive et statistique du peuplement zooplanctonique de la region de Nosy-bé (Madagascar). Doctoral thesis, Universitè d’Aix-Marseille II, France

    Google Scholar 

  • Gacia E, Costalago D, Prado P, Piorno D, Tomas F (2009) Mesograzers in Posidonia oceanica meadows: an update of data on gastropod-epiphyte-seagrass interactions. Bot Mar 52:439–447. doi:10.1515/BOT.2009.054

    Article  CAS  Google Scholar 

  • Gallmetzer I, Pflugfelder B, Zekely J, Ott JA (2005) Macrofauna diversity in Posidonia oceanica detritus: distribution and diversity of mobile macrofauna in shallow sublittoral accumulations of Posidonia oceanica detritus. Mar Biol 147:517–523. doi:10.1007/s00227-005-1594-9

    Article  Google Scholar 

  • Greenacre M (2007) Correspondence analysis in practice, 2nd edn. Chapman and Hall CRC Press, London

    Book  Google Scholar 

  • Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843. doi:10.1038/nature01416

    Article  CAS  Google Scholar 

  • Havelange S, Lepoint G, Dauby P, Bouquegnau JM (1997) Feeding of the sparid fish Sarpa salpa in a seagrass ecosystem: diet and carbon flux. PSZNI Mar Ecol 18:289–297. doi:10.1111/j.1439-0485.1997.tb00443.x

    Article  Google Scholar 

  • Ianora A, Bentley MG, Caldwell GS, Casotti R, Cembella AD, Engström-Öst J, Halsband C, Sonnenschein E, Legrand C, Llewellyn CA, Paldavičienë A, Pilkaityte R, Pohnert G, Razinkovas A, Romano G, Tillmann U, Vaiciute D (2011) The relevance of marine chemical ecology to plankton and ecosystem function: an emerging field. Mar Drug 9:1625–1648. doi:10.3390/md9091625

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jones RH, Flynn KJ (2005) Nutritional status and diet composition affect the value of diatoms as copepod prey. Science 307:1457–1459. doi:10.1126/science.1107767

    Article  CAS  Google Scholar 

  • Jüttner F (1988) Quantitative analysis of volatile organic-compounds. Methods Enzymol 167:609–616

    Article  Google Scholar 

  • Jüttner F (1999) Allelochemical control of natural photoautotrophic biofilms. In: Keevil CW, Godfree A, Holt D, Dow C (eds) Biofilms in aquatic environment. Royal Society of Chemistry, Cambridge, pp 43–50

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Lane JQ, Roddam CM, Langlois GW, Kudela RM (2010) Application of solid phase adsorption toxin tracking (SPATT) for field detection of the hydrophilic phycotoxins domoic acid and saxitoxin in coastal California. Limnol Oceanogr Methods 8:645–660. doi:10.4319/lom.2010.8.645

    Article  CAS  Google Scholar 

  • Lauritano C, Borra M, Carotenuto Y, Biffali E, Miralto A, Procaccini G, Ianora A (2011) Molecular evidence of the toxic effects of diatom diets on gene expression patterns in copepods. PLoS One 6(10):e26850. doi:10.1371/journal.pone.0026850.g001

    Article  CAS  Google Scholar 

  • Lauritano C, Carotenuto Y, Miralto A, Procaccini G, Ianora A (2012) Copepod population-specific response to a toxic diatom diet. PLoS One 7(10):e47262. doi:10.1371/journal.pone.0047262

    Article  CAS  Google Scholar 

  • Leflaive J, Ten-Hage L (2009a) Chemical interactions in diatoms: role of polyunsaturated aldehydes and precursors. New Phytol 184:794–805. doi:10.1111/j.1469-8137.2009.03033.x

    Article  CAS  Google Scholar 

  • Leflaive J, Ten-Hage L (2009b) Allelopathic interactions in benthic biofilms: effects of abiotic conditions on production of and sensitivity to allelochemicals. J N Am Benthol Soc 28:273–282. doi:10.1899/08-039.1

    Article  Google Scholar 

  • Legrand C, Rengefors K, Fistarol GO, Graneli E (2003) Allelopathy in phytoplankton–biochemical, ecological and evolutionary aspects. Phycologia 42:406–419. doi:10.2216/i0031-8884-42-4-406.1

    Article  Google Scholar 

  • Lepoint G, Cox AS, Dauby P, Poulicek M, Gobert S (2006) Food sources of two detritivore amphipods associated with the seagrass Posidonia oceanica leaf litter. Mar Biol Res 2:355–365. doi:10.1080/17451000600962797

    Article  Google Scholar 

  • Mazzella L, Russo GF (1989) Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves. Aquat Bot 35:353–373. doi:10.1016/0304-3770(89)90007-7

    Article  Google Scholar 

  • Miralto A, Barone G, Romano G, Poulet SA, Ianora A, Russo GL, Buttino I, Mazzarella G, Laabir M, Cabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 402:173–176. doi:10.1038/46023

    Article  CAS  Google Scholar 

  • Nappo M, Berkov S, Codina C, Avila C, Messina P, Zupo V, Bastida J (2009) Metabolite profiling of the benthic diatom Cocconeis scutellum by GC-MS. J Appl Phycol 21:295–306. doi:10.1007/s10811-008-9367-8

    Article  CAS  Google Scholar 

  • Pagano G, Cipollaro M, Corsale G, Esposito A, Ragucci E, Giordano GG, Trieff NM (1986) The sea urchin: bioassay for the assessment of damage from environmental contaminants. In: Cairns J (ed) Community toxicity testing. American Society for Testing and Materials, Philadelphia, pp 66–92

    Chapter  Google Scholar 

  • Peduzzi P (1987) Dietary preferences and carbon absorption by two grazing gastropods: Gibbula umbilicaris and Jujubinus striatus. PSZNI Mar Ecol 8:359–370. doi:10.1111/j.1439-0485.1987.tb00194.x

    Article  Google Scholar 

  • Pohnert G (2000) Wound-activated chemical defence in unicellular planktonic algae. Angew Chem Int Ed 39:4352–4355. doi:10.1002/1521-3773(20001201

    Article  CAS  Google Scholar 

  • Pohnert G (2004) Chemical defense strategies of marine organisms. In: Schulz S (ed) The chemistry of pheromones and other semiochemicals I, Springer, Top Curr Chem 239, pp 179–219. doi:10.1007/b95453

  • 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

    Article  Google Scholar 

  • Poulet SA, Cueff A, Wichard T, Marchetti J, Dancie C, Pohnert G (2007) Influence of diatoms on copepod reproduction. III. Consequences of abnormal oocyte maturation on reproductive factors in Calanus helgolandicus. Mar Biol 152(2):415–428. doi:10.1007/s00227-007-0701-5

    Article  Google Scholar 

  • Prince EK, Poulson KL, Myers TL, Sieg RD, Kubanek J (2010) Characterization of allelopathic compounds from the red tide dinoflagellate Karenia brevis. Harmful Algae 10:39–48. doi:10.1016/j.hal.2010.06.003

    Article  CAS  Google Scholar 

  • Raniello R, Iannicelli MM, Nappo M, Avila C, Zupo V (2007) Production of Cocconeis neothumensis (Bacillariophyceae) biomass in batch cultures and bioreactors for biotechnological applications: light and nutrient requirements. J Appl Phycol 19:383–391. doi:10.1007/s10811-006-9145-4

    Article  CAS  Google Scholar 

  • Romano G, Russo GL, Buttino I, Ianora A, Miralto A (2003) A marine diatom-derived aldehyde induces apoptosis in copepod and sea urchin embryos. J Exp Biol 206:3487–3494. doi:10.1242/jeb.00580

    Article  Google Scholar 

  • Romano G, Miralto A, Ianora A (2010) Teratogenic effects of diatom metabolites on sea urchin Paracentrotus lividus embryos. Mar Drug 8:950–967. doi:10.3390/md8040950

    Article  CAS  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge

    Google Scholar 

  • Scipione MB, Gambi MC, Lorenti M, Russo GF, Zupo V (1996) Vagile fauna of the leaf stratum of Posidonia oceanica and Cymodocea nodosa in the Mediterranean Sea. In: Kuo J, Phillips RC, Walker DI, Kirkman H (eds) Seagrass biology: proceedings of an international workshop. The University of Western Australia, Nedlands, pp 249–260

    Google Scholar 

  • Steele JH (1974) The structure of marine ecosystems. Blackwell Scientific Harvard University Press, Cambridge, Massachusetts, Oxford

    Book  Google Scholar 

  • Steigenberger S, Statham PJ, Voelker C, Passow U (2010) The role of polysaccharides and diatom exudates in the redox cycling of Fe and the photoproduction of hydrogen peroxide in coastal seawaters. Biogeosciences 7:109–119. doi:10.5194/bg-7-109-2010

    Article  CAS  Google Scholar 

  • Stevenson RJ, Peterson CG, Kirschtel DB, King CC, Tuchman NC (1991) Density-dependent growth, ecological strategies, and effects of nutrients and shading on benthic diatom succession in streams. J Phycol 27:59–69. doi:10.1111/j.0022-3646.1991.00059.x

    Article  Google Scholar 

  • Sunda WG, Shertzer KW (2012) Modeling ecosystem disruptive algal blooms: positive feedback mechanisms. Mar Ecol Prog Ser 447:31–69. doi:10.3354/meps09482

    Article  CAS  Google Scholar 

  • Takada Y, Russo GF, Mazzella L (1999) Activity pattern and habitat preference of two herbivorous gastropods (Gibbula umbilicaris and Jujubinus striatus) on leaves of the Mediterranean seagrass Posidonia oceanica. Benthos Res 54:71–80

    Google Scholar 

  • Taylor RL, Abramsson K, Godhe A, Wangberg SA (2009) Seasonal variability in polyunsaturated aldehyde production potential among strains of Skeletonema marinoi (Bacillariophyceae). J Phycol 45:46–53. doi:10.1111/j.1529-8817.2008.00625.x

    Article  CAS  Google Scholar 

  • Taylor RL, Caldwell GS, Olive PJW, Bentley MG (2012) The harpacticoid copepod Tisbe holothuriae is resistant to the insidious effects of polyunsaturated aldehyde-producing diatoms. J Exp Mar Biol Ecol 413:30–37. doi:10.1016/j.jembe.2011.11.024

    Article  Google Scholar 

  • van Montfrans J, Orth RJ, Vay SA (1982) Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquat Bot 14:75–89. doi:10.1016/0304-3770(82)90087-0

    Article  Google Scholar 

  • Vidoudez C, Pohnert G (2008) Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi. J Plankton Res 30:1305–1313. doi:10.1093/plankt/fbn085

    Article  CAS  Google Scholar 

  • 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 Inform 1:23–32. doi:10.1016/j.ecoinf.2005.06.001

    Article  Google Scholar 

  • Watson SB, Ridal J (2004) Periphyton: a primary source of widespread and severe taste and odour. Water Sci Technol 49:33–39

    CAS  Google Scholar 

  • Wichard T, Poulet SA, Halsband-Lenk C, Albaina A, Harris R, Liu D, Pohnert G (2005a) 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

    Article  CAS  Google Scholar 

  • Wichard T, Poulet SA, Pohnert G (2005b) Determination and quantification of alpha, beta, gamma, delta-unsaturated aldehydes as pentafluorobenzyl-oxime derivates in diatom cultures and natural phytoplankton populations: application in marine field studies. J Chromatogr B 814:155–161. doi:10.1016/j.jchromb.2004.10.021

    Article  CAS  Google Scholar 

  • Wichard T, Poulet SA, Boulesteix AL, Ledoux JB, Lebreton B, Marchetti J, Pohnert G (2008) Influence of diatoms on copepod reproduction. II. Uncorrelated effects of diatom-derived alpha, beta, gamma, delta-unsaturated aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the field. Prog Oceanogr 77:30–44. doi:10.1016/j.pocean.2008.03.002

    Article  Google Scholar 

  • Wittmann K, Scipione MB, Fresi E (1981) Some laboratory experiments on the activity of the macrofauna in the fragmentation of detrital leaves of Posidonia oceanica (L.) Delile. Rapp Comm Int Mer Médit 27:205–206

    Google Scholar 

  • Zupo V (2000) Effect of microalgal food on the sex reversal of Hippolyte inermis (Crustacea: Decapoda). Mar Ecol Prog Ser 201:251–259

    Article  Google Scholar 

  • Zupo V, Messina P (2006) How do dietary diatoms cause the sex reversal of the shrimp Hippolyte inermis Leach (Crustacea, Decapoda). Mar Biol 151:907–917. doi:10.1007/s00227-006-0524-9

    Article  Google Scholar 

  • Zupo V, Messina P, Buttino I, Sagi A, Avila C, Nappo M, Bastida J, Codina C, Zupo S (2007) Do benthic and planktonic diatoms produce equivalent effects in crustaceans? Mar Freshw Behav Physiol 40:1–13. doi:10.1080/10236240701592930

    Article  Google Scholar 

  • Zupo V, Jüttner F, Maibam C, Butera E, Blom JF (2014) Apoptogenic metabolites in fractions of the benthic diatom Cocconeis scutellum parva. Mar Drug 12:547–567. doi:10.3390/md12010547

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Our research was supported by a Stazione Zoologica Anton Dohrn PhD course, within the Open University fellowship to C. Maibam under the supervision of V. Zupo and by an EU Assemble Marine Grant (No. 1060/G6) to P. Fink. This work has been 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. We acknowledge all the staff of the Benthic Ecology group of SZN for the assistance during the bioassays. Prof. M. De Stefano gave suggestions for the interpretation of diatom ecology and distribution in P. oceanica. Four anonymous reviewers definitely improved the quality of the original manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valerio Zupo.

Additional information

Communicated by U. Sommer.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maibam, C., Fink, P., Romano, G. et al. Relevance of wound-activated compounds produced by diatoms as toxins and infochemicals for benthic invertebrates. Mar Biol 161, 1639–1652 (2014). https://doi.org/10.1007/s00227-014-2448-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2448-0

Keywords

Navigation