Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T05:39:59.710Z Has data issue: false hasContentIssue false

Multitrophic Interactions in the Sea: Assessing the Effect ofInfochemical-Mediated Foraging in a 1-d Spatial Model

Published online by Cambridge University Press:  28 November 2013

N. D. Lewis*
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK Department of Mathematical Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK
A. Morozov
Affiliation:
Department of Mathematics, University of Leicester, Leicester, LE1 7RH, UK
M. N. Breckels
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK
M. Steinke
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK
E. A. Codling
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK Department of Mathematical Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

The release of chemicals following herbivore grazing on primary producers may providefeeding cues to carnivorous predators, thereby promoting multitrophic interactions. Inparticular, chemicals released following grazing on phytoplankton by microzooplanktonherbivores have been shown to elicit a behavioural foraging response in carnivorouscopepods, which may use this chemical information as a mechanism to locate and remainwithin biologically productive patches of the ocean. In this paper, we use a 1D spatialreaction-diffusion model to simulate a tri-trophic planktonic system in the water column,where predation at the top trophic level (copepods) is affected by infochemicals releasedby the primary producers forming the bottom trophic level. The effect of theinfochemical-mediated predation is investigated by comparing the case where copepodsforage randomly to the case where copepods adjust their vertical position to follow thedistribution of grazing-induced chemicals. Results indicate that utilization ofinfochemicals for foraging provides fitness benefits to copepods and stabilizes the systemat high nutrient load, whilst also forming a possible mechanism for phytoplankton bloomformation. We also investigate how the copepod efficiency to respond to infochemicalsaffects the results, and show that small increases (2%) in the ability of copepods tosense infochemicals can promote their persistence in the system. Finally we argue thateffectively employing infochemicals for foraging can be an evolutionarily stable strategyfor copepods.

Type
Research Article
Copyright
© EDP Sciences, 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Archer, S. D., Stelfox-Widdicombe, C. E., Burkill, P. H., Malin, G.. A dilution approach to quantify the production of dissolved dimethylsulphoniopropionate and dimethylsulphide due to microzooplankton herbivory. Aquat. Microb. Ecol., 23 (2001), 131145. CrossRefGoogle Scholar
Beckmann, A., Hense, I.. Beneath the surface: characteristics of oceanic ecosystems under weak mixing conditions — a theoretical investigation. Prog. Oceanogr., 75 (2007), 771796. CrossRefGoogle Scholar
Breckels, M. N., Bode, N. W. F., Codling, E. A., Steinke, M.. The effect of grazing-mediated DMS production on the behaviour of the copepod Calanus helgolandicus. Mar. Drugs, 11 (2013), 24862500. CrossRefGoogle ScholarPubMed
Charlson, R. J., Lovelock, J. E., Andreae, M. O., Warren, S. G.. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326 (1987), 655661. CrossRefGoogle Scholar
Chattopadhyay, J., Sarkar, R. R., Mandal, S.. Toxin producing plankton may act as a biological control for planktonic blooms-field study and mathematical modelling. J. Theor. Biol., 215 (2002), 333-344. CrossRefGoogle Scholar
Cowles, T. J., Desiderio, R. A., Carr, M. E.. Small scale planktonic structure: persistence and trophic consequences. J. Oceanogr., 11 (1998), 49. CrossRefGoogle Scholar
Cunningham, G. B., Strauss, V., Ryan, P. G.. African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey related cue. J. Exp. Biol., 211 (2008), 31233127. CrossRefGoogle Scholar
U. Dieckmann. Adaptive dynamics of pathogen-host interactions. In: Dieckmann, U, Metz, JAJ, Sabelis, M.W., Sigmund, K. (Eds.), Adaptive Dynamics of Infectious Diseases:In Pursuit of Virulence Management, Cambridge University Press, (2002), pp. 39–59.
Edwards, C. A., Batchelder, H. P., Powell, T. M.. Modeling microzooplankton and macrozooplankton dynamics within a coastal upwelling system. J. Plankton Res., 22 (2000), 16191648. CrossRefGoogle Scholar
Edwards, C. A., Powell, T. A., Batchelder, H. P.. The stability of an NPZ model subject to realistic levels of vertical mixing. J. Mar. Res., 58 (2000), 3760. CrossRefGoogle Scholar
Edwards, A. M., Brindley, J.. Zooplankton mortality and the dynamical behaviour of plankton population models. Bull. Math. Biol., 61 (1999), 303339. CrossRefGoogle ScholarPubMed
Farnsworth, K. D., Beecham, J. A.. How do grazers achieve their distribution? A continuum of models from random diffusion to the ideal free distribution using biased random walks. Am. Nat., 153 (1999), 509526. CrossRefGoogle Scholar
Gabric, A., Murray, N., Stone, L., Kohl, M.. Modelling the production of dimethylsulfide during a phytoplankton bloom. J. Geophys. Res., 98 (1993), 2280522816. CrossRefGoogle Scholar
Geritz, S.A.H., Kisdi, E., Meszena, G., Metz, J.A.J., Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol., 12, (1998), 3557. CrossRefGoogle Scholar
Gill, C. W., Poulet, S. A.. Responses of copepods to dissolved free amino acids. Mar. Ecol. Prog. Ser., 43 (1988), 269276. CrossRefGoogle Scholar
Giske, J., Rosland, R., Berntsen, J., Fiksen, Ø.. Ideal free distribution of copepods under predation risk. Ecol. Model., 95 (1997), 4559. CrossRefGoogle Scholar
Hansen, F.C., Reckermann, M., Klein Breteler, W.C.M.. Phaeocystis blooming enhanced by copepod predation on protozoa: evidence from incubation experiments. Mar. Ecol. Prog. Ser., 102 (1993), 5157. CrossRefGoogle Scholar
Hay, M. E.. Marine chemical ecology: chemical signals and cues structure marine populations, communities and ecosystems. Annu. Rev. Mar. Sci., 1 (2009), 193212. CrossRefGoogle Scholar
Holling, C. S.. The components of predation as revealed by a study of small mammal predation on the European pine sawfly. Can. Entomol., 91 (1959), 293320. CrossRefGoogle Scholar
Irigoien, X., Flynn, K. J., Harris, R. P.. Plankton blooms: a ’loophole’ in microzooplankton grazing impact? J. Plankton Res., 27 (2005), 313321. CrossRefGoogle Scholar
A. Kharab, R. B. Guenther. An Introduction to Numerical Methods: A MATLAB Approach. Third edition. CRC Press, Boca Raton, 2012.
T. Kiørboe. A Mechanistic Approach to Plankton Ecology. Princeton University Press, NJ, 2008.
Kiørboe, T., Bagøien, E., Thygesen, U. H.. Blind dating—mate finding in planktonic copepods. II. the pheromone cloud of Pseudocalanus elongatus. Mar. Ecol. Prog. Ser., 300 (2005), 117128. CrossRefGoogle Scholar
C. J. Krebs. Ecology. Sixth edition. Pearson, San Francisco, 2009.
Lampert, W.. Vertical distribution of zooplankton: density dependence and evidence for an ideal free distribution with costs. BMC Biol., 3 (2005), 10. CrossRefGoogle ScholarPubMed
Lewis, W. M.. Evolutionary interpretations of allelochemical interactions in phytoplankton algae. Am. Nat., 127 (1986), 184194. CrossRefGoogle Scholar
Lewis, N. D., Breckels, M. N., Archer, S. D., Morozov, A., Pitchford, J. W., Steinke, M., Codling, E. A.. Grazing-induced production of DMS can stabilize food-web dynamics and promote the formation of phytoplankton blooms in a multitrophic plankton model. Biogeochemistry, 110 (2012), 303313. CrossRefGoogle Scholar
N. D. Lewis, M. N. Breckels, M. Steinke, E. A. Codling. Role of infochemical mediated zooplankton grazing in a phytoplankton competition model. Ecol. Complex., (2012), http://dx.doi.org/10.1016/j.ecocom.2012.10.003.
MATLAB. The Language of Technical Computing, version 7.8. Mathworks, Natick, MA.
Montagnes, D. J. S., Berges, J. A., Harrison, P. J., Taylor, F. J. R.. Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton. Limnol. Oceanogr., 39 (1994), 10441060. CrossRefGoogle Scholar
Morozov, A., Arashkevich, E., Towards a correct description of zooplankton feeding in models: Taking into account food-mediated unsynchronized vertical migration. J. Theor. Biol., 262 (2010), 346360. CrossRefGoogle ScholarPubMed
Morozov, A., Arashkevich, E., Nikishina, A., Solovyev, K.. Nutrient-rich plankton community stabilized via predator-prey interactions: revisiting the role of vertical heterogeneity. Math. Med. Biol., 28 (2011), 185215. CrossRefGoogle Scholar
Nejstgaard, J. C., Båmstedt, U., Bagøien, E., Solberg, P. T.. Algal constraints on copepod grazing. Growth state, toxicity, cell size, and season as regulating factors. ICES J. Mar. Sci., 52 (1995), 347357. CrossRefGoogle Scholar
Nejstgaard, J. C., Gismervik, I., Solberg, P. T.. Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser., 147 (1997), 197217. CrossRefGoogle Scholar
Nevitt, G. A., Veit, R. R., Kareiva, P.. Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds. Nature, 376 (1995), 680682. CrossRefGoogle Scholar
Pohnert, G., Lumineau, O., Cueff, A., Adolph, S., Cordevant, C., Lange, M., Poulet, S.. Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods?. Mar. Ecol. Prog. Ser., 245 (2002), 3335. CrossRefGoogle Scholar
Pohnert, G., Steinke, M., Tollrian, R.. Chemical cues, defense metabolites and the shaping of pelagic interspecific interactions. Trends Ecol. Evol., 22 (2007), 198204. CrossRefGoogle Scholar
Poulet, S. A., Ouellet, G.. The role of amino acids in the chemosensory swarming and feeding of marine copepods. J. Plankton Res., 4 (1982), 341361. CrossRefGoogle Scholar
Rosenzweig, M. L.. Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science, 171 (1971), 385387. CrossRefGoogle ScholarPubMed
Rosenzweig, M. L., MacArthur, R. H.. Graphical representation and stability conditions of predator-prey interactions. Am. Nat., 97 (1963), 209223. CrossRefGoogle Scholar
Ryabov, A. B., Blasius, B.. A graphical theory of competition on spatial resource gradients. Ecol. Lett 14 (2011), 220228. CrossRefGoogle ScholarPubMed
Ryabov, A. B.. Phytoplankton competition in deep biomass maximum. Theor. Ecol., 5 (2012), 373385. CrossRefGoogle Scholar
Saltzman, E. S., King, D. B., Holmen, K., Leck, C.. Experimental determination of the diffusion coefficient of dimethylsulfide in water. J. Goephys. Res., 98 (1993), 1648116486. CrossRefGoogle Scholar
Shaw, B. A., Andersen, R. J., Harrisen, P.J.. Feeding deterrence properties of apo-fucoxanthinoids from marine diatoms. I. Chemical structures of apo-fucoxanthinoids produced by Phaeodactylum tricornutum. Mar. Biol., 124 (1995), 467472. CrossRefGoogle Scholar
Shaw, B. A., Harrison, P. J., Andersen, R. J.. Feeding deterrence properties of apo-fucoxanthinoids from marine diatoms. II. Physiology of production of apo-fucoxanthinoids by the marine diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana, and their feeding deterrence effects on the copepod Tigriopus californicus. Mar. Biol., 124 (1995), 473481. CrossRefGoogle Scholar
Stefels, J., Steinke, M., Turner, S., Malin, G., Belviso, S.. Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling. Biogeochemistry, 83 (2007), 245275. CrossRefGoogle Scholar
Steinke, M., Malin, G., Archer, S. D., Burkill, P. H., Liss, P. S.. DMS production in a coccolithophorid bloom: evidence for the importance of dinoflagellate DMSP lyases. Aquat. Microb. Ecol., 26 (2002), 259270. CrossRefGoogle Scholar
Steinke, M., Malin, G., Liss, P.S.. Trophic interactions in the sea: an ecological role for climate relevant volatiles? J. Phycol., 38 (2002), 630638. CrossRefGoogle Scholar
Steinke, M., Stefels, J., Stamhuis, E.. Dimethyl sulfide triggers search behaviour in copepods. Limnol. Oceanogr., 51 (2006), 19251930. CrossRefGoogle Scholar
Sunda, W., Kieber, D. J., Kiene, R. P., Huntsman, S.. An antioxidant function for DMS and DMSP in marine algae. Nature, 418 (2002), 317320. CrossRefGoogle ScholarPubMed
D. Tilman. Resource Competition and Community Structure. Princeton University Press, Princeton, NJ.
Tiselius, P.. Behaviour of Acartia tonsa in patchy food environments. Limnol. Oceanogr., 37 (1992), 16401651. CrossRefGoogle Scholar
Turner, J. T., Tester, P. A.. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr., 42 (1997), 12031214. CrossRefGoogle Scholar
Visser, A. W., Kiørboe, T.. Plankton motility patterns and encounter rates. Oecologia, 148 (2006), 538546. CrossRefGoogle ScholarPubMed
Wolfe, G. V., Steinke, M.. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol. Oceanogr., 41 (1996), 11511160. CrossRefGoogle Scholar
Woodson, C. B., Webster, D. R., Weissburg, M. J., Yen, J.. Cue hierarchy and foraging in calanoid copepods: ecological implications of oceanographic structure. Mar. Ecol. Prog. Ser., 330 (2007), 163177. CrossRefGoogle Scholar
Yamazaki, H., Squires, K. D.. Comparison of oceanic turbulence and copepod swimming. Mar. Ecol. Prog. Ser., 144 (1996), 299301. CrossRefGoogle Scholar
Yen, J., Rasberry, K. D., Webster, D. R.. Quantifying copepod kinematics in a laboratory apparatus. J. Mar. Syst., 69 (2008), 283294. CrossRefGoogle Scholar