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Determinants of Seasonal Feeding of the Generalist Snail Arianta Ar- Bustorum at Six Sites Dominated by Senecioneae

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Determinants of Seasonal Feeding of the Generalist Snail Arianta Ar- Bustorum at Six Sites Dominated by Senecioneae Published in Oecologia 128, issue 2, 228-236, 2001 1 which should be used for any reference to this work Determinants of seasonal feeding of the generalist snail Arianta ar- bustorum at six sites dominated by Senecioneae Bernd F. Hägele · Martine Rahier Abstract We investigated the diet constituents of Ari- Keywords Snails · Secondary plant compounds · Food anta arbustorum by means of faecal analysis and re- quality · Food availability · Senecioneae gressed their quantity on the availability and quality of food plants. We studied six sites, all dominated by plants from the Asteraceae tribe Senecioneae, early and later in Introduction the growing season, predicting that the snail’s food choice would be determined by the presence of the dif- Feeding by any animal will primarily serve to meet its ferent secondary compounds found in the Senecioneae. basic needs for nutrition. While in carnivores this can The snails consumed less green plant material and more usually be done without ingesting other unwanted diet leaf litter in May than in July. Plant water and nitrogen constituents, herbivores face the problem that in addition content were higher in May. For the May samples, re- to the low and mostly unbalanced nutrient content of gressions were only significant at sites that excluded their diet, it almost always comes with added feeding Adenostyles alliariae and Adenostyles alpina; in July, the deterrents, digestibility reducers or even toxic compo- regression fit was higher at all sites. Of the measured nents (Crawley 1983; Strong et al. 1984; Simpson and plant parameters, only quantity (availability) was a con- Simpson 1990; Bernays and Chapman 1994). While spe- sistently significant variable in the regressions. Circum- cialised herbivores have evolved effective countermea- stantial evidence suggested that plant secondary com- sures to deal with these added complications to their nu- pounds had a major influence on snail food choice: trition, and some may even use them to their own advan- fresh-plant consumption increased over the season, as tage against their predators (Rowell-Rahier and Pasteels the concentration of many secondary compounds de- 1992; Rowell-Rahier et al. 1995), generalist herbivores, creased; both plant availability and quality could only although capable of efficient detoxification (Brattsten explain about half of the observed variation in snail feed- 1992), are thought to be more affected by constitutive or ing, which argues for other hidden factors influencing induced secondary plant compounds (van der Meijden snail feeding; the dynamics of feeding of the various se- 1996; Karban and Baldwin 1997). Specialisation in her- necionean plants were such that A. alliariae and Senecio bivores has been fundamental in the predictions for the sp. had a seasonal acceptance whereas Petasites albus evolution of levels of plant defensive compounds, their was always and A. alpina never accepted, and, finally, dynamics and their characteristics with regard to plant the detection of a number of snail-deterrent fractions in life history (Feeny 1976; Rhoades and Cates 1976; A. alpina leaves, a plant which was never found to be Bryant et al. 1983; Coley et al. 1985; Feeny 1990; consumed in this study. van der Meijden 1996). In some cases, predictions of these types of hypotheses have been confirmed (e.g. B.F. Hägele (✉) Bryant et al. 1989), whereas in others, the evidence has Universität Basel, Zoologisches Institut, Rheinsprung 9, been only partially supportive (e.g. Hägele and Rowell- 4052 Basel, Switzerland Rahier 1999b). M. Rahier Research on slugs and snails as generalist herbivores, Université de Neuchâtel, Institut de Zoologie, although less extensive than in insects and vertebrates, Rue Emile Argand 11, 2007 Neuchâtel, Switzerland has a long tradition in herbivore biology. In fact, one of Present address: the first comprehensive studies on the effect of plant sec- B.F. Hägele, Université de Neuchâtel, Institut de Zoologie, Rue Emile Argand 11, 2007 Neuchâtel, Switzerland, ondary compounds on herbivore feeding was done with e-mail: [email protected] slugs and snails (Stahl 1888). However, except for some Tel.: +41-32-7183068, Fax: +41-32-7183001 slugs, most snails have omnivorous feeding habits, in- 2 Table 1 Pattern of pyrrolizidine alkaloid (PA) and sesquiterpene compounds, leading to hypotheses about acceptance or avoidance (ST) content of asteracean plants, known feeding response of Ari- of a plants during the season anta arbustorum to Adenostyles alliariae and some secondary Plant Early season Late season Hypotheses on References species snail feeding Adenostyles High concentrations of Low concentrations of Seasonal avoidance Speiser and Rowell-Rahier 1991; alliariae non-deterrent PAs; non-deterrent PAs; (dependent on non-PA Hägele 1992; Hägele et al. 1996; low concentrations of low concentration of secondary compounds) Hägele and Rowell-Rahier 1999b snail-deterrent STs; snail-deterrent STs; avoided by A. arbustorum accepted by A. arbustorum Adenostyles Low concentrations of Unknown concentrations General avoidance due Hägele 1992; Hägele et al. 1996; alpina non-deterrent PAs; of non-deterrent PAs; to ST content Hägele and Rowell-Rahier 1999b low concentrations of increased concentrations additional deterrent STs of additional deterrent STs Senecio sp. Low concentrations of Unknown concentrations (Partial) avoidance? Seaman 1982; Rowell-Rahier non-deterrent PAs; of non-deterrent PAs; et al. 1991 unknown concentrations of unknown concentrations of STs with untested effects STs with untested effects Petasites No PAs; unknown No PAs; unknown Acceptance Rowell-Rahier et al. 1991; albus concentrations of non- concentrations of Hägele et al. 1996 deterrent STs non-deterrent STs cluding fungi, and senescent and decaying plant material deterrent effect of the plant alkaloid content. This inter- into their diet (Frömming 1937, 1962; Chang 1991). pretation had to be withdrawn, when alkaloids them- Since the nutritional value of decaying plant material is selves were found to have no snail-deterrent effect impoverished (through bacterial and fungal decomposi- (Speiser et al. 1992). However, the discovery that sesqui- tion), the benefits of feeding on decomposing material terpenes from A. alliariae were snail deterrent (Speiser might lie in increased palatability as secondary plant et al. 1992; Hägele et al. 1996, 1998) prompted further chemicals are also broken down. Nevertheless, fresh investigation. By comparing sites dominated by different plant material should be most nutritionally valuable for senecionean plant species, we wanted to test the hypo- the herbivore. For the plant, only the loss of green pro- thesis that qualitative constitutive defences determine ductive leaf mass should have (fitness) consequences, snail food choice. and therefore fresh leaf mass should be protected as a Based on our knowledge about the major secondary valuable resource (McKey 1979; Mattson 1980; Herms compounds of the Senecioneae, pyrrolizidine alkaloids and Mattson 1992). (PAs) and sesquiterpenes (STs), we hypothesised that we The importance of snails as generalist herbivores can could expect different feeding patterns according to the only be determined by field studies, measuring their im- presence or absence of the plant compounds (see pact on the existing plant community. However, direct Table 1). We specifically asked whether (1) plant avail- observation of feeding in the field is complicated by ability was the major predictor of snail feeding over the the partially nocturnal activity of snails and their being variety of habitats investigated, (2) there was seasonal easily disturbed by an approaching observer, causing variation in feeding as predicted by our knowledge of the them to withdraw into the shell and become inactive. occurrence of plant compounds, and (3) plant nutritious Therefore faecal analysis of snails, sampled in a given quality, measured as water, carbon, nitrogen, sugar and area, is an appropriate way to investigate their diet, pro- starch content, rather than secondary compounds, could viding an indirect record of all feeding events throughout predict a significant part of the variability in snail feeding. a given time period, determined by the speed that food items pass through the dietary system (Speiser and Rowell-Rahier 1991). An experimental approach using Materials and methods artificially created systems with a defined species com- position is a very useful method to determine the impor- We collected 22–30 adult snails of the species Arianta arbustorum tance of snail herbivory under specific circumstances, (L.) (Gastropoda, Helicidae) at each of six field sites early and late but it can never mimic the field situation with its interac- in the growing season. We tried to sample exhaustively in the smallest possible area. A. arbustorum is the most common helicid tions at all trophic levels (Fraser and Grime 1999). snail in middle Europe (Kaestner 1982) and is common in humid In their field study, Speiser and Rowell-Rahier (1991) habitats up to 2,700 m in altitude (Kerney et al. 1983). Each snail found that plant availability was the only significant fac- was placed into a small plastic container (4 cm diameter, 2.5 cm tor explaining part of the variability in snail feeding. high) lined with moist white toilet paper. Snail faeces were regu- larly removed from the containers until the paper faeces appeared, They also found evidence for a seasonal change in palat- which was usually after 1–2 days. This
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