Geophytes–herbivore interactions: reproduction and population dynamics of Anemone coronaria L. Plant Ecology An International Journal ISSN 1385-0237 Volume 212 Number 4 Plant Ecol (2011) 212:563-571 DOI 10.1007/ s11258-010-9846-2 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Plant Ecol (2011) 212:563–571 DOI 10.1007/s11258-010-9846-2 Geophytes–herbivore interactions: reproduction and population dynamics of Anemone coronaria L. A. Perevolotsky • R. Schwartz-Tzachor • R. Yonathan • G. Ne’eman Received: 16 August 2009 / Accepted: 17 September 2010 / Published online: 5 November 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Anemone coronaria, an attractive Medi- grazing increased biomass and height of the herba- terranean geophyte, seems to disappear from grazing- ceous community and reduced relative PAR at ground protected areas in Israel. We experimentally examined level. Consequently, seedling, adult plant and flower- the ecological mechanism driving the decline of this ing Anemone plant densities were lower in ungrazed geophyte. Ten plot-pairs were established, half we plots. We recommend adding seasonal grazing as a fenced as grazing exclosures and half were grazed by management tool when vegetation outcompete light beef cattle. Grazing clearly reduced herbaceous bio- demanding geophytes that we wish to conserve. mass, increased relative solar photosynthetic active radiation (PAR) at ground level, but had almost no Keywords Competition Á Conservation Á Grazing Á effect on soil properties. Grazing did not affect the Light Á Livestock Á Mediterranean number of flowers and young fruits produced by A. coronaria, nor the percentage fruit-set at the plot scale, indicating no effect on flowering, pollination, or Introduction on resource allocation to reproduction. Five years after grazing exclusion, Anemone seedling and adult plant Grazing by wildlife or domesticated animals is gener- densities were higher in grazed than in ungrazed plots. ally considered as a disturbance to grazed plants. We propose a model explaining our results that can be According to Grime (1979), grazing is ‘the total or applied also to other similar ecosystems: excluding partial destruction of plant biomass that arises from the activities of herbivores’. Others consider grazing as a stress factor restricting photosynthetic production A. Perevolotsky Á R. Yonathan (Dyer et al. 1993). Grazing, or its exclusion, has been Department of Agronomy and Natural Resources, ARO—The Volcani Center, Bet Dagan, Israel recognized as a factor that can mould and shape plant e-mail: [email protected]; [email protected] community composition and structure (Crawley 1983; Todd and Hoffman 1999; Milchunas and Noy-Meir R. Schwartz-Tzachor 2002). The contemporary approach considers abiotic Nature-Park Ramat Hanadiv, Zikhron Ya’akov, Israel e-mail: [email protected] conditions, competition and herbivory as prominent factors affecting community structure (Wardle and G. Ne’eman (&) Barker 1997); this is especially valid in areas that Department of Science Education-Biology, have been exposed to heavy utilization by livestock Faculty of Science and Science Education, University of Haifa-Oranim, Tivon 36006, Israel for millennia (Perevolotsky and Seligman 1998). e-mail: [email protected] Heavy grazing may also affect ecosystem abiotic 123 Author's personal copy 564 Plant Ecol (2011) 212:563–571 characteristics (van der Koppel et al. 1997) such as Israel. They suggested that grazing may release the erosion (Mwendra and Saleem 1997), soil structure light-mediated competitive inhibition of geophytes by (Proffitt et al. 1995) and productivity (Williams and their surrounding herbaceous vegetation, but did not Haynes 1995). present any supportive empirical data. An extensive Grazing may have differing impacts on plant correlative survey that monitored the relations species due to herbivore preference or plant resis- between grazing exclusion and geophyte abundance tance (McIntyre et al. 1995; Dumont 1997: Lavorel in northern Israel demonstrated higher geophyte et al. 1997). Perennial species, with long growing density in grazed than in neighbouring ungrazed sites season, tall, erect or bulky structure, are preferred by (Noy-Meir and Oron 2001). In Israel, 107 geophyte grazers over small, prostrate species with short life species grow in open well-light Mediterranean habi- cycle (Noy-Meir et al. 1989; Fernandez et al. 1993), tats, whereas only 14 species grow in shady woodlands and plants that develop chemical or morphological (Fragman and Shmida 1997), and negative effects of defence are grazed less than plants with less effective tree-shading on geophytes density (Hadar et al.1999) deterrents (Grubb 1992). and flowering (Oz and Dafni 1991; Ne’eman 2003) Geophytes are perennial herbaceous plants that were demonstrated by tree removal. However, no shed their leaves during seasons unfavourable for experimental study has examined the direct or indirect growth (cold, dry), but resume growth from under- effects of grazing on a target geophyte in an herba- ground storage organs in the next season (Raunkiaer ceous community, proposing and testing an ecological 1934). Tyler and Borchert (2002) suggest that mechanism. geophyte diversity is highest in Mediterranean type We hypothesized that grazing has a positive ecosystems comprising 16% of the diverse Cape flora indirect effect on flowering, reproductive success and (Goldblat 1997) and 9% (217 species) of the Israeli population density of A. coronaria by reducing the flora (Fragman and Shmida 1997). Many geophytes light-mediated competition with the surrounding her- in Israel are rare, considered sensitive to disturbance, baceous vegetation. To test this hypothesis we exper- and therefore require special conservation efforts. imentally examined the effect of cattle grazing on the Following many years of traditional flower picking, relationship between A. coronaria and its surrounding geophytes with conspicuous flowers are now pro- herbaceous vegetation. Specifically we asked: what is tected under Israeli law. the effect of grazing on Anemone flowering, fruit-set, Anemone coronaria L. (Feibrun-Dothan and Danin seedling, adult and flowering-plant densities, since 1991) is a geophyte with massive and attractive these parameters determine the long-term persistence flowering during winter and early spring; it is common of the species in the community. in open Mediterranean landscapes that are often used for livestock grazing (Koniak et al. 2009). A. coronaria in Israel is colour polymorphic, red flowers are most Materials and methods common (Shmida and Dafni 1989; Dafni et al. 1990), but white, pink, blue and violet flowers also occur in Study area the same or different populations. Some of those populations served as stocks for A. coronaria cultivars This study was conducted at the Ramat Hanadiv Park, grown in gardens (Horovitz et al. 1975a, b; Horovitz located at the southern tip of Mount Carmel in and Danin 1983). A. coronaria is largely avoided by northern Israel, about 5 km from the Mediterranean mammalian herbivores, probably due to the toxins sea-shore, at 150 m above sea level. The climate in protoanemonin (Knight and Walter, 2001) and anem- the region is mild Mediterranean; the winter is short, onin (Cheeke 1998) that gave the plant its scientific wet and cool, and the summer is long, rainless and name. Currently, A. coronaria populations seem to hot. Average annual rainfall is 600 mm, and it occurs decrease in grazing-protected areas but not in open mostly during November–March. Various formations rangelands in Israel. of limestone and dolomite compose the bedrock in Naveh and Whittikar (1979) were the first to the park, and the common soil is Xerochreps, locally observe a positive effect of grazing on geophyte known as Terra-Rossa. The vegetation is a typical diversity in Mediterranean plant communities in Mediterranean shrubland (also known as phrygana or 123 Author's personal copy Plant Ecol (2011) 212:563–571 565 garrigue) dominated by the shrubs Phillyrea latifolia two or more leaves) and of flowering A. coronaria L., Calycotome villosa L. and Pistacia lentiscus L. plants were measured. and accompanied by Sarcopoterium spinosum L. Spach dwarf shrubs. Open patches of various sizes Statistical analyses with herbaceous vegetation occur among the shrubs and this is the local habitat of A. coronaria. To reduce variations due to plot location, we designed Since 1985, the park has been committed to the plots in pairs and used paired t-tests to compare sustainable development and ecologically sound variables between grazed and ungrazed plots, where management. Four to six months of cattle grazing we made several measurements of the same variable during January–June is regularly used to reduce in one plot, and the plot average was used for further herbaceous and woody biomass, as fire prevention analyses. To examine differences among years we management (Perevolotsky et al. 2003). used repeated measures one-way ANOVA for the grazed and ungrazed plots separately. All variables Experimental design and measurements that were proportions were transformed (y = square root [arcsin(x)]) before analysis. We used SPSS 11.0.1 In January 1997, we assigned ten pairs of experi- to analyze the data. mental plots (2 9 3 m each) and fenced one of each plot-pair to exclude grazing. We monitored all A. coronaria plants in each plot every 10–14 days Results during the growing seasons (mid-December to mid- April, 1997–2002) counting the plants, the flowers, Exclusion of heavy cattle grazing for 3 years had no young fruits and fruits at seed dispersal stage per significant effects on soil pH, conductivity, P and K.