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Aphid herbivory as a potential driver of primary succession in coastal dunes

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Abstract

Herbivory is a major factor affecting both the performance and the fitness of the species composing a plant community and, ultimately, conditioning its temporal and spatial dynamics. Coastal dunes are a typical example of primary succession where different biotic and abiotic factors determine plant species occurrence; however, the effect of insect herbivory herein has remained little explored. To address this matter, we combined an observational study along a successional gradient with a green-house experiment to determine the occurrence and the impact of plant–aphid interactions. We focused on the species Schizaphis rufula, a widespread and abundant aphid associated with dune grasses in early stages of primary succession in Europe. Firstly, we studied aphid infestation rates on the dune grass Ammophila arenaria along a succession gradient in three locations of the North Sea coast to address the relationship between plant community composition and aphid occurrence; secondly, we tested the effect of aphid herbivory on a set of dune species typical for the different stages of succession. We found that the degree of aphid infestation was inversely correlated with the degree of dune fixation. The results of the experiment showed that aphid multiplication was significantly higher and its effect more pronounced on two early successional grass species, i.e. A. arenaria and Leymus arenarius. Here aphid multiplication resulted in a severe decrease in plant biomass; in late successional grass species, there was limited multiplication and no effect on biomass. The results of the field survey and the green-house experiment indicate that aphids show a clear preference for plants from early successional stages and, moreover, they have a greater impact on these plant species. All this supports the hypothesis of aphid herbivory as a driving factor of primary succession in coastal dunes.

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References

  • Allan E, Crawley MJ (2011) Contrasting effects of insect and molluscan herbivores on plant diversity in a long-term field experiment. Ecol Lett 14:1246–1253. doi:10.1111/j.1461-0248.2011.01694.x

    Article  PubMed  Google Scholar 

  • Bach CE (1994) Effects of a specialist herbivore (Altica Subplicata) on Salix cordata and sand dune succession. Ecol Monogr 64:423–445

    Article  Google Scholar 

  • Bach CE (2001) Long-term effects of insect herbivory and sand accretion on plant succession on sand dunes. Ecology 82:1401–1416

    Article  Google Scholar 

  • Bai Y, Wu J, Clark CM, Pan Q, Zhang L, Chen S, Wang Q, Han X (2012) Grazing alters ecosystem functioning and C:N: P stoichiometry of grasslands along a regional precipitation gradient. J Appl Ecol 49:1204–1215. doi:10.1111/j.1365-2664.2012.02205.x

    Article  CAS  Google Scholar 

  • Bertels L, Deronde B, Kempeneers P, Provoost S, Tortelboom E (2005) Potentials of airborne hyperspectral remote sensing for vegetation mapping of spatial heterogeneous dynamic dunes—a case study along the Belgian coastline. In: Herrier J-L, Mees J, Salman A, Seys J, Van Nieuwenhuyse H, Dobbelaere I (eds) Proceedings ‘Dunes and Estuaries 2005’—international conference on nature restoration practices in European coastal habitats. Koksijde, Belgium, pp 153–163

    Google Scholar 

  • Bezemer TM, De Deyn GB, Bossinga TM, Van Dam NM, Harvey JA, van der Putten WH (2005) Soil community composition drives aboveground plant–herbivore–parasitoid interactions. Ecol Lett 8:652–661. doi:10.1111/j.1461-0248.2005.00762.x

    Article  Google Scholar 

  • Bond TET (1952) Biological flora of the British Isles: Elymus arenarius L. J Ecol 40:217–227

    Article  Google Scholar 

  • Borer ET, Seabloom EW, Mitchell CE, Cronin JP (2014) Multiple nutrients and herbivores interact to govern diversity, productivity, composition, and infection in a successional grassland. Oikos 123:214–224. doi:10.1111/j.1600-0706.2013.00680.x

    Article  Google Scholar 

  • Börner C, Heinse K (1957) Aphidina—Aphidoidea. In: Sorauer P (ed) Handbuch der Pflanzenkrankheiten, 5th edn. Paul Parey, Berlin, pp 1–402

    Google Scholar 

  • Brinkman EP, Duyts H, van der Putten WH (2005) Consequences of variation in species diversity in a community of root-feeding herbivores for nematode dynamics and host plant biomass. Oikos 110:417–427

    Article  Google Scholar 

  • Brinkman EP, Duyts H, Karssen G, van der Stoel CD, van der Putten WH (2015) Plant-feeding nematodes in coastal sand dunes: occurrence, host specificity and effects on plant growth. Plant Soil 397:17–30. doi:10.1007/s11104-015-2447-z

    Article  CAS  Google Scholar 

  • Choeni H, Sebata A (2014) Interspecific variation in the resprouting responses of Acacia species following simulated herbivory in a semi-arid southern African savannah. Afr J Ecol 52:479–483. doi:10.1111/aje.12149

    Article  Google Scholar 

  • Clark LR (1964) The population dynamics of Cardiaspina albitextura (Psyllidae). Aust J Zool 12:362–380

    Article  Google Scholar 

  • Colwell RK (2009) Biodiversity: concepts, patterns, and measurement. In: Levin LA (ed) The Princeton guide to ecology. Princeton University Press, Princeton, pp 257–264. doi:10.1111/j.1442-9993.2012.02436.x

  • Connel J, Slatyer R (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  • Crevits H (2008) Natuurrichtplan voor de VEN-gebieden, speciale beschermingszone, groen-, park- en bosgebieden in de “Duinen van de Middenkust tussen Oostende en Blankenberge”, tekstbijlage. Belgisch Staatsblad, Brussels, pp 1–69

    Google Scholar 

  • de la Peña E, Rodríguez Echeverría S, Van Der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169(4):829–840

    Article  PubMed  Google Scholar 

  • de la Peña E, Bonte D, Moens M (2009) Evidence of population differentiation in the dune grass Ammophila arenaria and its associated root-feeding nematodes. Plant Soil 324:307–316

    Article  Google Scholar 

  • de la Peña E, Vandomme V, Frago E (2014) Facultative endosymbionts of aphid populations from coastal dunes of the North Sea. Belg J Zool 144:41–50

    Google Scholar 

  • De Rooij-van der Goes PCEM (1995) The role of plant-parasitic nematodes and soil-borne fungi in the decline of Ammophila arenaria (L.) Link. New Phytol 129:661–669

    Article  Google Scholar 

  • Evidente A, Andolfi A, Cimmino A, Ganassi S, Altomare C, Favilla M, De Cristofaro A, Vitagliano S, Sabatini MA (2009) Bisorbicillinoids produced by the fungus Trichoderma citrinoviride affect feeding preference of the aphid Schizaphis graminum. J Chem Ecol 35:533–541. doi:10.1007/s10886-009-9632-6

    Article  CAS  PubMed  Google Scholar 

  • Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Func Ecol 25:399–407

    Article  Google Scholar 

  • Fraser LH, Grime JP (1999) Interacting effects of herbivory and fertility on a synthesized plant community. J Ecol 87:514–525

    Article  Google Scholar 

  • Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039. doi:10.1111/j.1461-0248.2009.01356.x

    Article  PubMed  Google Scholar 

  • Hågvar EB, Hofsvang T (1991) Aphid parasitoids (Hymenoptera, Aphidiidae): biology, host selection and use in biological control. Biocontrol News Inf 12:13–41

    Google Scholar 

  • Herrier J-L, Mees J, Salman A, Seys J, Van Nieuwenhuyse H, Dobbelaere I (eds) (2005) Proceedings ‘Dunes and Estuaries 2005’: international conference on nature restoration practices in European coastal habitats, Koksijde, Belgium 19–23 September 2005. VLIZ Special Publication, 19. Vlaams Instituut voor de Zee (VLIZ), Oostende, pp XIV-685

  • Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ, Harpole WS, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909. doi:10.1073/pnas.0701918104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horgan FG, Stuart AM, Kudavidanage EP (2014) Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecol 54:90–100. doi:10.1016/j.actao.2012.10.002

    Article  Google Scholar 

  • Huiskes AHL (1979) Biological flora of the British Isles: Ammophila arenaria (L.) link (Psamma arenaria (L.) Roem. et Shult.; Calamagrostis arenaria (L.) Roth). J Ecol 67:363–382

    Article  CAS  Google Scholar 

  • Huston M, Smith T (1987) Plant succession: life history and competition. Am Nat 130:168–198

    Article  Google Scholar 

  • Ibanez S, Bison M, Lavorel S, Moretti M (2013) Herbivore species identity mediates interspecific competition between plants. Community Ecol 14:41–47. doi:10.1556/ComEc.14.2013.1.5

    Article  Google Scholar 

  • Imbert E, Houle G (2001) Spatio-temporal dynamics of root mass density in a coastal dune in subarctic Quebec, Canada. J Coast Res 17:877–884

    Google Scholar 

  • Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848. doi:10.1111/j.1461-0248.2007.01073.x

    Article  PubMed  Google Scholar 

  • Kaplan I, Sardanelli S, Rehill BJ, Denno RF (2011) Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia 166:627–636. doi:10.1007/s00442-010-1885-9

    Article  PubMed  Google Scholar 

  • Karlsen SR, Jepsen JU, Odland A, Ims RA, Elvebakk A (2013) Outbreaks by canopy-feeding geometrid moth cause state-dependent shifts in understorey plant communities. Oecologia 173:859–870. doi:10.1007/s00442-013-2648-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuijper DPJ, Jedrzejewska B, Brzeziecki B, Churski M, Jedrzejewski W, Zybura H (2010) Fluctuating ungulate density shapes tree recruitment in natural stands of the Białowieza Primeval Forest, Poland. J Veg Sci 21:1082–1098. doi:10.1111/j.1654-1103.2010.01217.x

    Article  Google Scholar 

  • Lichter J (2000) Colonization constraints during primary succession on coastal Lake Michigan sand dunes. J Ecol 88:825–839

    Article  Google Scholar 

  • Long ZT, Mohler CL, Carson WP (2003) Extending the resource concentration hypothesis to plant communities: effects of litter and herbivores. Ecology 84:652–665

    Article  Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc Biol Sci 273:2575–2584. doi:10.1098/rspb.2006.3587

    Article  PubMed  PubMed Central  Google Scholar 

  • Massad TJ (2013) Ontogenetic differences of herbivory on woody and herbaceous plants: a meta-analysis demonstrating unique effects of herbivory on the young and the old, the slow and the fast. Oecologia 172:1–10. doi:10.1007/s00442-012-2470-1

    Article  PubMed  Google Scholar 

  • Maun MA (2009) Plant communities. In: Maun MA (ed) The biology of coastal sand dunes. Oxford University Press, New York, pp 164–180

    Google Scholar 

  • Moorleghem C (2014) Unraveling the ecology of the dune aphid Schizaphis rufula (Hemiptera: Aphidoidea): ecological preferences and parasitoids (Hymenoptera). MSc. Dissertation, Department of Biology, University of Ghent, Ghent, pp 42

  • Nickel H, Remane R (2002) Artenliste der Zikaden Deutschlands, mit Angabe von Nährpflanzen, Nahrungsbreite, Lebenszyklus, Areal und Gefährdung (Hemiptera, Fulgoromorpha et Cicadomorpha). Beiträge zur Zikadenkunde 5:27–64

    Google Scholar 

  • Nieto Nafría JM (2007) Fauna Europaea: Hemiptera, Aphidoidea. Fauna Europaea version 1.3. http://www.faunaeur.org. Accessed 15 May 2014

  • Pettersson J (1971a) Studies on four grass-inhabiting species of Schizaphis (Hem. Aphidoidea) with special reference to sex habits of S. arrhenatheri Pettersson. Dissertation, Swedish University of Agricultural Sciences

  • Pettersson J (1971b) Studies on four grass-inhabiting species of Schizaphis (Hem. Aphidoidea): I. Literature review. Ent Scand 2:67–73

    Article  Google Scholar 

  • Pettersson J (1971c) Studies on four grass-inhabiting species of Schizaphis (Hom.: Aph.): III. (a) host plants. Swed J Agric Res 1:133–138

    Google Scholar 

  • Pimentel D (1961) Species diversity and insect population outbreaks. Ann Entomol Soc Am 54:422–437

    Article  Google Scholar 

  • Provoost S, Feys S, Van Gompel W, Vercruysse W (2011a) Evaluatie van het gevoerde beheer en opmaak van een beheerplan voor het VNR De Duinen en Bossen van De Panne. Deel I: Evaluatie van het gevoerde beheer in de deelgebieden Houtsaegerduinen en de Westhoek. Rapporten van het Instituut voor Natuur- en Bosonderzoek 53, Instituut voor Natuur- en Bosonderzoek, Brussel, pp 123

  • Provoost S, Jones MLM, Edmondson SE (2011b) Changes in landscape and vegetation of coastal dunes in northwest Europe: a review. J Coast Conserv 15:207–226

    Article  Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica Oleracea). Ecol Monogr 43:95–124. doi:10.2307/1942161

    Article  Google Scholar 

  • SAS Institute Inc (2014) SAS/STAT® 9.4 user’s guide. SAS Institute Inc, Cary, pp 272

  • Schmitz OJ (2008) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152. doi:10.1146/annurev.ecolsys.39.110707.173418

    Article  Google Scholar 

  • Stam JM, Kroes A, Li Y, Gols R, van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713. doi:10.1146/annurev-arplant-050213-035937

    Article  CAS  PubMed  Google Scholar 

  • Starý P (1987) Subject bibliography of aphid parasitoids (Hymenoptera: Aphidiidae) of the world 1758–1982. Monogr Appl Entomol 25:101

    Google Scholar 

  • Stein C, Unsicker SS, Kahmen A, Wagner M, Audorff V, Auge H, Prati D, Weisser WW (2010) Impact of invertebrate herbivory in grasslands depends on plant species diversity. Ecology 91:1639–1650. doi:10.1890/09-0600.1

    Article  PubMed  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. doi:10.1016/S0169-5347(98)01576-6

    Article  PubMed  Google Scholar 

  • Tariq M, Wright DJ, Rossiter JT, Staley JT (2012) Aphids in a changing world: testing the plant stress, plant vigour and pulsed stress hypotheses. Agric For Entomol 14:177–185. doi:10.1111/j.1461-9563.2011.00557.x

    Article  Google Scholar 

  • Turpeau E, Hullé M, Chaubet B (2013) Caractères généraux des cycles. Encyclop’Aphid. https://www6.inra.fr/encyclopedie-pucerons/Qu-est-ce-qu-un-puceron/Cycles-biologiques. Accessed 22 April 2014

  • Unsicker SB, Baer N, Kahmen A, Wagner M, Buchmann N, Weisser WW (2006) Invertebrate herbivory along a gradient of plant species diversity in extensively managed grasslands. Oecologia 150:233–246. doi:10.1007/s00442-006-0511-3

    Article  PubMed  Google Scholar 

  • van der Putten WH, Troelstra SR (1990) Harmful soil organisms in coastal foredunes involved in degeneration of Ammophila arenaria and Calammophila baltica. Can J Bot Rev Can Bot 68:1560–1568

    Article  Google Scholar 

  • van der Putten WH, Breteler JTV, Van Dijk C (1989) Colonization of the root zone of Ammophila arenaria by harmful soil organisms. Plant Soil 120:213–223

    Article  Google Scholar 

  • Van der Stoel CD, van der Putten WH, Duyts H (2002) Development of a negative plant-soil feedback in the expansion zone of the clonal grass Ammophila arenaria following root formation and nematode colonization. J Ecol 90:978–988

    Article  Google Scholar 

  • Van der Stoel CD, Duyts H, van der Putten WH (2006) Population dynamics of a host-specific root-feeding cyst nematode and resource quantity in the root zone of a clonal grass. Oikos 112:651–659

    Article  Google Scholar 

  • van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208

    Article  PubMed  Google Scholar 

  • Vandegehuchte ML, de la Peña E, Bonte D (2010a) Relative importance of biotic and abiotic soil components to plant growth and insect herbivore population dynamics. PLoS ONE 5:e12937. doi:10.1371/journal.pone.0012937

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandegehuchte ML, de la Peña E, Bonte D (2010b) Aphids on Ammophila arenaria in Belgium: first reports, phenology and host range expansion. Belg J Zool 140:77–80

    Google Scholar 

  • Vandegehuchte ML, de la Peña E, Bonte D (2010c) Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos 119:1011–1019. doi:10.1111/j.1600-0706.2009.18360.xVan

    Article  Google Scholar 

  • Weeda EJ, Westra R, Westra C, Westra T (2003) Nederlandse oecologische flora: wilde planten en hun relaties 5. KNNV Uitgeverij/IVN, Zeist, p 400

    Google Scholar 

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Acknowledgments

Eduardo de la Peña thanks the support of the Ramón y Cajal programme (RYC-2012-10254, Spanish Ministry of Economy and Competitiveness. This study was also supported by the programme Europa Investigación 2015 (EUIN2015-62833). We thank the Nature Reserve Westhoek, and all the staff at the Terrestrial Ecology group of Ghent University and Eline Vermote for their help during the course of this study and two anonymous reviewers for their helpful comments on the manuscript. We thank Prof. Jan Pettersson for sending to us his original works on the genus Schizaphis.

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  1. Terrestrial Ecology Unit, Department of Biology, Faculty of Sciences, University of Ghent, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Charlotte Van Moorleghem & Eduardo de la Peña

  2. Laboratory for Functional Morphology, Department of Biology, Faculty of Sciences, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium

    Charlotte Van Moorleghem

  3. Institute for Mediterranean and Subtropical Horticulture “La Mayora” (IHSM-UMA-CSIC), 29750, Algarrobo-Costa, Málaga, Spain

    Eduardo de la Peña

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  1. Charlotte Van Moorleghem
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  2. Eduardo de la Peña
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Correspondence to Eduardo de la Peña.

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Van Moorleghem, C., de la Peña, E. Aphid herbivory as a potential driver of primary succession in coastal dunes. Arthropod-Plant Interactions 10, 89–100 (2016). https://doi.org/10.1007/s11829-016-9421-4

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