Oecologia (2005) 146: 227–233 DOI 10.1007/s00442-005-0192-3 PLANTANIMALINTERACTIONS Martin Scha¨dler Æ Mareike Roeder Æ Roland Brandl Diethart Matthies Is palatability of a root-hemiparasitic plant influenced by its host species? Received: 16 November 2004 / Accepted: 21 June 2005 / Published online: 19 July 2005 Ó Springer-Verlag 2005 Abstract Palatability of parasitic plants may be influ- Introduction enced by their host species, because the parasites take up nutrients and secondary compounds from the hosts. If Parasitic plants attack shoots or roots of other plants and parasitic plants acquired the full spectrum of secondary take up water, nutrients and solutes from the hosts by compounds from their host, one would expect a corre- means of specialized contact organs (haustoria, Kuijt lation between host and parasite palatability. We 1969). About 1% of all plants are parasitic and parasitic examined the palatability of leaves of the root-hemi- plants are common components of many plant commu- parasite Melampyrum arvense grown with different host nities (Molau 1995). The majority of parasitic plants are plants and the palatability of these host plants for two actually hemiparasites that have green leaves and are generalist herbivores, the caterpillar of Spodoptera lit- able to photosynthesize (Kuijt 1969). Parasitic plants can toralis and the slug Arion lusitanicus. We used 19 species drastically reduce the growth of their host plants and of host plants from 11 families that are known to con- some are important agricultural pests (Parker and Riches tain a wide spectrum of anti-herbivore compounds. 1993; Pennings and Callaway 2002). Because parasitic Growth of M. arvense was strongly influenced by the plants are to a certain degree host-specific, they may host species. The palatability of the individual host mediate competitive interactions between different host species for the two herbivores differed strongly. Both A. plants and thus influence community structure (Matthies lusitanicus and S. littoralis discriminated also between 1996; Joshi et al. 2000; Pennings and Callaway 2002; hemiparasites grown with different host plants. There Pywell et al. 2004). was no correlation between the palatability of a host The parasitic way of life may have other benefits for species and that of the parasites grown on that host, i.e., the parasites apart from providing access to resources hemiparasites grown on palatable host species were not like water, nutrients and carbohydrates from the host more palatable than those grown on unpalatable hosts. plant. Parasitic plants can also take up secondary com- We suggest an interacting pattern of specific effects of pounds produced by their hosts that act as anti-herbivore chemical anti-herbivore defences and indirect effects of defences (Schneider and Stermitz 1990; Boros et al. the hosts on herbivores through effects on growth and 1991). Several studies of specific host–parasite pairs tissue quality of the parasites. found that these compounds are taken up by the parasite and reduce its herbivory levels (Harvey 1966; Marvier Keywords Melampyrum arvense Æ Herbivory Æ 1996; Adler et al. 2001; Adler 2002, 2003). For example, Host–parasite interactions Æ Secondary compounds quinolizidine alkaloids taken up by the root hemiparasite Castilleja indivisa from high-alkaloid Lupinus albus re- duced herbivory levels and increased lifetime seed set of Communicated by Christian Koerner the parasites in comparison to parasites grown with low- alkaloid lupines (Adler 2000). Insect larvae suffered M. Scha¨ dler Æ R. Brandl higher mortalities when fed with fruits of the root Department of Animal Ecology, Faculty of Biology, hemiparasite Santalum acuminatum that had grown near University of Marburg, Karl-von-Frisch-Str., 35032 Melia azedarach Marburg, Germany the host than when fed with fruits from parasites growing away from M. azedarach (Loveys et al. M. Roeder Æ D. Matthies (&) 2001). Department of Plant Ecology, Faculty of Biology, University of Marburg, Karl-von-Frisch-Str., 35032 Marburg, However, no attempt has been made to study the ef- Germany fect of a wide range of hosts on the palatability of a E-mail: matthies@staff.uni-marburg.de parasitic plant. If parasitic plants take up indiscrimi- 228 nately a wide spectrum of secondary compounds from of the days when the feeding trials were conducted. their host plant, the palatability of a parasite and its host While S. littoralis is a standard test organism in pal- should be correlated. We studied the influence of hosts atability trials and does not occur together with M. from 11 plant families, most of them known to produce arvense, A. lusitanicus may be regarded as a potential secondary compounds that may deter herbivores, on the herbivore of this species in the field. palatability of the root hemiparasite Melampyrum ar- We selected a total of 19 host plant species from 11 vense L. for two generalist herbivores, the slug Arion lu- families (Table 1). These included plants known to sitanicus and the caterpillar of Spodoptera littoralis.We contain a wide spectrum of secondary compounds that addressed the following specific questions: (1) Do the may negatively affect generalist herbivores and some different host species influence the palatability of the species that are not or poorly defended by secondary parasitic plant for generalist herbivores? (2) Is the pal- compounds (Poaceae, some Fabaceae). Seeds of the host atability of the hemiparasite correlated with that of its species were sown in standard potting soil (TKS 1, host? Floragard, Oldenburg/Germany, 110 mg lÀ1 N, À1 À1 130 mg l P2O5, 180 mg l K2O) in October 2002. Seedlings were transplanted into individual pots Materials and methods (9 cm·9cm·9.5 cm) filled with the same soil in January 2003. The temperature in the glasshouse was 20–30°C M. arvense (Scrophulariaceae) is an obligate root during the day and 15–20°C at night. Day length was hemiparasite that without a host dies during the early maintained at 14 h, with additional light supplied by stages of development (Matthies 1995). The annual high-pressure sodium lamps (Philips, Son-T Agro, species was formerly a noxious weed of cereal fields in 400 W). Thirty to 40 replicates were prepared for every Europe but has become rare due to changes in agricul- host species. Once per week, a 0.2% solution of an tural practices. Today, M. arvense is a plant of calcare- NPK-fertilizer (8-8-6, Wuxal super, Aglukon Du¨ ssel- ous grasslands and field margins (Matthies 1986). dorf) was applied to the plants. Two generalist herbivores were used in our study. Seedlings of M. arvense were germinated at the The cotton leafworm S. littoralis (Boisduval) (Lepi- beginning of December 2002 in Petri dishes on moist doptera: Noctuidae) is a serious pest of several crops filter paper in a climate chamber at 4°C to break dor- in North Africa, the Mediterranean and the Middle mancy. After 3 weeks, the temperature was raised to East (Sadek 2003). The caterpillars of this moth attack 8°C. When the parasites had fully developed their cot- host plants belonging to at least 40 plant families yledons in March 2003, two individuals of M.arvense (Brown and Dewhurst 1975). The species was bred were planted into half of the pots with the host species. under laboratory conditions on lettuce and welled During the following 2 weeks, pots with hemiparasites white beans. The slug Arion lusitanicus (Mollusca: were placed in a climate chamber at 18°C/15°C (day/ Agriolimacidae) is a widespread invasive herbivore night) and a day length of 16 h to facilitate the estab- introduced from Southern Europe. In Central Europe, lishment of seedlings. During this time, dead hemipar- the slug feeds on a wide range of plant species (Briner asites were replaced by new seedlings before pots were and Frank 1998). Slugs were sampled in the sur- brought back to the glasshouse. In mid-April 2003, all rounding of the institute in Marburg in the mornings pots were moved to a flowerbed in the Botanical Gar- Table 1 List of host plant species used in the experiments Host species Family Secondary compounds Longevity with information on important secondary compounds known Achillea millefolium Asteraceae Sesquiterpenic lactones Perennial to occur in the plant tissue Agrostemma githago Caryophyllaceae Steroid saponins Annual (taken from Hoppe 1958; Roth Arrhenatherum elatius Poaceae No defensive compounds known Perennial et al. 1994, and the Atropa belladonna Solanaceae Alkaloids (atropin) Perennial toxicological data base of the Chelidonium majus Papaveraceae Alkaloids Perennial University of Zu¨ rich at http:// Cicuta virosa Apiaceae Cicutoxin Perennial www.vetpharm.unizh.ch). Conium maculatum Apiaceae Alkaloids (e.g., coniin) Biennial Taxonomy of plants follows Digitalis purpurea Scrophulariaceae Glucosides Biennial Schmeil and Fitschen (1996) Euphorbia platyphyllos Euphorbiaceae Triterpene saponines, Euphorbon Annual and Roth et al. (1994). Species Genista germanica Fabaceae Alkaloids Perennial are in alphabetical order Lobelia inflata Campanulaceae Alkaloids Annual Lotus corniculatus Fabaceae Cyanogenic glucoside Perennial Lupinus angustifolius Fabaceae Alkaloids Annual Lupinus luteus Fabaceae None (low-alkaloid line) Annual Melilotus alba Fabaceae Coumarine-glucoside, Annual, biennial Cyanogenic glucoside Nicotiana tabacum Solanaceae Alkaloids (nicotin) Annual Ricinus communis Euphorbiaceae Proteins Annual Sinapis alba Brassicaceae Glucosinolates (sinalbin) Annual Trifolium repens Fabaceae Cyanogenic glucosides Perennial 229 den, where light conditions and temperatures were more squares in the analyses, the effect of host species on favourable for the growth of the parasites. After one feeding was analysed after removing the possibly con- month of growth, the height, number of leaves and the founding influence of individual herbivore size, and size length and width of the longest leaf were determined for and nutritive status of the hemiparasite. each hemiparasite. In addition, the water content was Since phylogenetically related taxa often contain determined for 80 leaves of M. arvense and 20 leaves of similar secondary compounds (Hendriks et al. 1999), we every host species.