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Insect Herbivory on Native and Exotic Aquatic Plants: Phosphorus and Nitrogen Drive Insect Growth and Nutrient Release

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Insect Herbivory on Native and Exotic Aquatic Plants: Phosphorus and Nitrogen Drive Insect Growth and Nutrient Release Hydrobiologia DOI 10.1007/s10750-015-2448-1 SHALLOW LAKES Insect herbivory on native and exotic aquatic plants: phosphorus and nitrogen drive insect growth and nutrient release Bart M. C. Grutters . Elisabeth M. Gross . Elisabeth S. Bakker Received: 15 April 2015 / Revised: 16 July 2015 / Accepted: 13 August 2015 Ó The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Eutrophication and globalisation facilitate stratiotata consumed seven out of eleven plant the dominance of exotic plants in aquatic ecosystems species, and their growth was related to plant nutrient worldwide. Aquatic omnivores can provide biotic content and stoichiometry. However, larvae had no resistance to plant invasions, but little is known about preference for either native or exotic macrophytes, and whether obligate aquatic herbivores can do the same. their plant preference was not related to the measured Herbivores such as insects can decimate aquatic plant traits, but was possibly driven by secondary vegetation, but may not be able to consume exotic metabolites. Through plant consumption, caterpillars plants due to their more or less specialised nature of induced brownification and phosphate release, and the feeding. We experimentally tested the larval feeding intensity thereof varied among plant species, but not of an aquatic insect, the moth Parapoynx stratiotata, between native and exotic plants. In conclusion, P. on eleven submerged plant species, from either native stratiotata showed strong feeding preferences demon- or exotic origin. We also tested whether insect strating that aquatic insects can directly and indirectly herbivory stimulates nutrient and organic matter alter water quality and vegetation composition. release, thus affecting water quality. Larvae of P. Keywords Aquatic caterpillar Á Crambidae Á Ecological stoichiometry Á Invasive plants Á Parapoynx stratiotata Water brownification Guest editors: M. Bekliog˘lu, M. Meerhoff, T. A. Davidson, Á K. A. Ger, K. E. Havens & B. Moss / Shallow Lakes in a Fast Changing World Introduction Electronic supplementary material The online version of this article (doi:10.1007/s10750-015-2448-1) contains supple- mentary material, which is available to authorized users. Eutrophication and globalisation cause a worldwide increase of invading exotic plants in aquatic ecosys- B. M. C. Grutters (&) Á E. S. Bakker tems (Meyerson & Mooney, 2007). Exotic plants are Department of Aquatic Ecology, Netherlands Institute of introduced through aquaculture and global plant trade Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands (Kay & Hoyle, 2001; Martin & Coetzee, 2011; e-mail: [email protected] Hussner, 2012) and they rank among the top four threats to freshwater biodiversity (Dudgeon et al., E. M. Gross 2006) with more than 96 invasive exotic aquatic plants Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), UMR 7360, Universite´ de Lorraine, already established in Europe (Hussner, 2012). They Campus Bridoux, 57070 Metz, France grow fast, disperse quickly and easily establish in 123 Hydrobiologia eutrophied ecosystems (Simberloff et al., 2011). As a Until now, herbivore preferences for exotic or result, plant invaders dominate many disturbed habi- native aquatic plant species have been mainly studied tats (MacDougall & Turkington, 2005; Simberloff using omnivorous animals. However, specialist her- et al., 2011). Notorious aquatic plant genera are bivores may suppress exotic plant growth better than Hydrilla (L.f.) Royle, Myriophyllum L. and Elodea omnivores, even though aquatic habitats contain fewer Michx., and their management costs millions of euros specialist herbivores than terrestrial habitats (New- annually (Langeland, 1996; Oreska & Aldridge, 2011; man, 1991; Harrison et al., 2008; Gross & Bakker, Zehnsdorf et al., 2015). An open question is whether 2012). More specialised herbivores can be effective native herbivores can provide biotic resistance to agents of biotic resistance, such as milfoil weevils plant invasions. This will depend strongly on herbi- (Euhrychiopsis lecontei Dietz) and the aquatic moth vore feeding preferences for certain plant species. Acentria ephemerella that consume exotic M. spica- There is contrasting evidence: native herbivores tum (Johnson et al., 1997, 2000; Solarz & Newman, preferred exotic aquatic plant species in several 2001). In addition, plants cannot easily recover from studies (Parker & Hay, 2005; Morrison & Hay, insect herbivory through regrowth, because many 2011), but preferred native plants in other studies insects target not only leaves, but also stems and apical (Xiong et al., 2008). We hypothesised that the meristems (Newman, 1991; Johnson et al., 1997, preference of native herbivores for certain plant 2000; Choi et al., 2002; Fornoff & Gross, 2014). The species is related to the plant quality. massive outbreak of insect herbivores can decimate Plant nutrient content may affect both the inva- dense stands of macrophytes and alter the plant species siveness of plants and their susceptibility to herbi- composition by direct feeding impacts (Johnson et al., vores. The growth rate hypothesis predicts that fast 1997, 2000; Gross et al., 2001). Furthermore, they can growth, often found in invasive plant species, requires indirectly affect vegetation composition by releasing rapid protein synthesis in plants, and much phospho- nutrients and organic compounds through excretion rus-rich RNA (Sterner & Elser, 2002). As both plant following the consumption of large amounts of and herbivore growths are limited mostly by nitrogen macrophytes (Newman, 1991; Vanni, 2002). The (N) and phosphorus (P) (Mattson, 1980; Barko & microbial degradation of dissolved organic com- Smart, 1986; Barko et al., 1988; Smith et al., 1999), pounds into humic acids can then cause brownification rapidly growing plants may be better food for herbi- of the water (Roulet & Moore, 2006; Graneli, 2012), vores than slow growing ones, because the N and P which affects light availability and vegetation com- contents of such plants are relatively high. For position (Mormul et al., 2012). example, rudd and grass carp prefer aquatic plants In this study, we assessed the preference of a with lower C:N ratios, resulting from a higher N herbivorous insect for native and exotic plant species, content (Dorenbosch & Bakker, 2011). Besides and we investigated how its consumption affects elemental stoichiometry, plants can differ in chemical nutrient release and water quality. We expected that feeding deterrents, and also in the ratio of deterrents to plant stoichiometry and nutrient content, but not plant feeding attractants (Cronin et al., 2002; Gross & origin, would explain herbivore preference and herbi- Bakker 2012). The aquatic caterpillar Acentria vore-induced effects on water quality. ephemerella Denis & Schiffermu¨ller can grow on the chemically well-defended M. spicatum, but it grows better on the more nutritious, less-defended P. perfo- Materials and methods liatus L. (Choi et al., 2002). Similarly, fish ate more of the well-defended M. spicatum when it contained Study species more nitrogen (Dorenbosch & Bakker, 2011). Inter- estingly, foliar traits differ between native and exotic The Ringed China-mark (Parapoynx stratiotata L. species (Penuelas et al., 2010). Therefore, native 1758; Crambidae) is a native European moth with an herbivores could potentially restrict exotic plant aquatic larval stage that requires host plants for habitat growth and allow growth of other plant species by and food (Lekic, 1971; Vallenduuk & Cuppen, 2004). selective consumption, if exotic plants are favoured Field observations showed that P. stratiotata can food items. decimate aquatic vegetation (Gaevskaya, 1969; 123 Hydrobiologia Spencer & Lekic, 1974), but apart from anecdotal served as experimental units. At the start of the evidence, little is known about the moth’s feeding experiment, we added plant portions to all trays, patterns, its growth and its effects on nutrient release. photographed them and then released caterpillars in We tested whether or not the palatability of native and half of the trays per plant species. Plant biomass was exotic macrophytes to P. stratiotata differs. Eleven abundant to allow unrestricted feeding during the macrophyte species were collected from experimental experiment. We placed all trays in a room (19°C) with ponds located at the Netherlands Institute of Ecology daylight and allowed larvae to feed for 96 h. Larvae (51.9880 N, 5.6720 E) in July 2013. These aquatic plants were then transferred to trays with fresh tap water are now all common in Northwestern Europe and where we waited for them to empty their gut (i.e. it was frequently form dense vegetation in eutrophic freshwa- not visibly green, brown or black) prior to freezing ters. We tested six native vascular plants: Myriophyllum them in Eppendorf tubes. Later we unfroze larvae, spicatum L., M. verticillatum L., Ranunculus circinatus dried them at 60°C and weighed them (mg dry mass). Sibth, Potamogeton lucens L., P. pusillus L. and We measured the carbon and nitrogen content of Ceratophyllum demersum L. and one native charophyte: caterpillars using a FLASH 2000 organic elemental Chara contraria ABraunexKu¨tzing. In addition, four analyser (Interscience BV, Breda, the Netherlands) exotic vascular plants were fed to caterpillars: M. and measured the phosphorus content by incinerating aquaticum (Vell.) Verdc. (native range: South America),
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