An experimental test for effects of the maternal environment on delayed germination

Transcription

1 Journl of Ecology 2010, 98, doi: /j x An experimentl test for effects of the mternl environment on delyed germintion Ktj Tielo rger* nd Mrtin Petru Deprtment of Plnt Ecology, University of Tu ingen, Auf der Morgenstelle 3, D Tu ingen, Germny Summry 1. Recent models on et-hedging germintion in nnul plnts ssume negtive reltionship etween the proportion of offspring tht germinte nd the qulity of the mternl environment. An increse in the proportion of seeds remining dormnt in the next yer, when produced in sesons with high reproduction my result from selection tht voids overcrowding in the following yer. 2. We present the first empiricl test of this prediction y utilizing field experiment in Isrel which mnipulted the entire mternl environment. We sujected semi-rid nd Mediterrnen nnul plnt communities to different rinfll tretments: control, reduced nd incresed rinfll. We then relted mternl environment qulity to offspring germintion frctions for three focl species in two consecutive sesons. 3. There ws negtive reltionship etween the qulity of the mternl environment nd offspring germintion frction in four out of twelve cses. The negtive reltionship ws stronger for the lest competitive species nd in the environment with high competition intensity, supporting the role of competition for the oserved pttern. 4. Our results suggest tht competition with ll neighours is more likely to explin the pttern thn si competition. 5. Synthesis. Our findings provide the first experimentl evidence of highly relile cue (productivity of mternl environment) tht llows for plnts to respond to their future iotic environment. There is n urgent need for testing predictions of theoreticl models in nturl popultions nd for incorporting the role of density dependence in studies of et-hedging germintion. Key-words: dptive strtegy, nnul plnts, et hedging, Biscutell didym, Bromus fscicultus, competition, field rinfll mnipultions, Hymenocrpos circinntus, predictive germintion, seed dormncy Introduction *Correspondence uthor. E-mil: ktj.tieloerger@uni-tueingen.de Seed dormncy in nnul plnts inhiting unpredictle environments llows voidnce of temporlly unfvourle conditions. By spreding germintion over severl sesons, extinction risk is reduced nd, on verge, plnts my exploit more fvourle conditions. Numerous studies hve modelled optiml germintion frctions of nnul plnts. Most of these were sed on the pioneering model of Cohen (1966), which ssumes tht germintion proilities of ll seeds in the seed nk re equl, constnt cross sesons, nd proportionl to the proility of experiencing fvourle seson. Lter studies hve extended this model nd relxed two of the most restrictive ssumptions. First, germintion rtes were llowed to vry ccording to environmentl cues indictive of the fvourility of the next seson (so-clled predictive germintion sensu Cohen 1967; Venle & Lwlor 1980; Ellner 1985). Secondly, Cohen s density-independent cse ws expnded to sitution, where siling competition reduces individul seed yield (Westoy 1981; Bulmer 1984; Ellner 1985,; Le on 1985; Ellner 1986, 1987; Nilsson et l. 1994; Koyshi & Ymmur 2000). While the numer of models on et-hedging germintion of nnuls is extremely lrge, empiricl evidence from nturl popultions testing their predictions hs lgged fr ehind (Philippi 1993,; Pke & Venle 1996; Cluss & Venle 2000; Venle 2007). A common ssumption of these models is homogeneous seed nk, i.e. t given time ll seeds in the soil shre the sme germintion proility. However, empiricl studies hve shown tht this ssumption is unrelistic ecuse germintion frctions my vry with respect to the rinfll history tht the seeds hve experienced, nd with the size nd fecundity of the mother plnt (Zmmit & Zedler 1990; Philippi 1993; Tielo rger & Vllerini 2005). Nevertheless, severl decdes Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society

2 Mternl environment effects on germintion 1217 pssed since Cohen s pioneering model efore it ws shown theoreticlly tht heterogeneous seed nks could e selected for (Tuljpurkr & Istock 1993; Tielo rger & Vllerini 2005; Vllerini & Tielo rger 2006). Such pttern my emerge, when predictive germintion is coupled with density-dependent seed yield. In this cse, seeds produced in fvourle (high yield) sesons should hve lower proportionl germintion thn seeds produced in unfvourle (low yield) sesons. This cn e explined s follows: if dormncy is higher fter fvourle sesons, the offspring my reduce negtive effects of crowding in the following yer (Tielo rger & Vllerini 2005; Vllerini & Tielörger 2006). In this context, one must properly distinguish etween two spects of crowding tht cn hve different evolutionry consequences. Most previous models hve focused on crowding mong sis of the sme prent, where higher dormncy incresed the fitness of the individul mother plnt y reducing the negtive effects of siling competition (e.g. Bulmer 1984; Ellner 1986). A conceptul derivtive of these models (the so-clled si-competition hypothesis), which ssumes heterogeneous seed nk, hs een tested empiriclly. The prediction of this hypothesis, which hs received some empiricl support in the field (Zmmit & Zedler 1990; wek support y Hytt & Evns 1998) nd in greenhouse studies (Philippi 1993), is tht seeds of mother plnts with mny seeds exhiit higher dormncy thn seeds from smll seed fmilies. Another spect of crowding includes competition mong ll plnts (intrspecific nd interspecific) in community. Becuse plnts use essentilly the sme resources nd ecuse most neighours re non-sis nd interspecific neighours rther thn sis lone, overll community (diffuse) competition should e much more importnt thn si competition. Also, the negtive consequence of this type of crowding is effective not only t n individul level. It lso reduces verge individul fitness in popultion nd therefore lso reduces popultion growth rte. Mechnisms to void generl competition thus serve not only to increse individul fitness ut lso to enhnce the long-term persistence of species. A recent model therefore proposed tht higher dormncy in seed fmilies tht were generted in fvourle yers resulted from competition mong ll seedlings, irrespective of their siship (Tielo rger & Vllerini 2005). The prediction of this model is negtive reltionship etween the qulity of the mternl environment nd the verge offspring germintion frction. One chllenge of studying predictive germintion (sensu Cohen 1967) empiriclly is to find relile cue of yer qulity tht cn e detected y the seed prior to germintion. Previous studies hve focused on iotic cues such s the first rinfll of seson. Usully there ws no positive correltion etween the first mjor rin event of seson tht triggers germintion nd the totl rinfll of seson (ut see Pke & Venle 1996). The intriguing consequence of the germintion models tht incorporte generl competition is tht community performnce in the previous yer cn e etter indictor of the current-yer qulity, t lest in terms of the iotic environment into which the seed will germinte (Tielörger & Vllerini 2005). The precise cue from community performnce tht gives rise to chnge in germintion rte could e relted to mny different spects of qulity in the mternl environment, oth iotic (e.g. competition) or iotic (e.g. wter, nutrient fluxes) (Pltenkmp & Shw 1993). Testing models of predictive germintion with generl density dependence rther thn with si-competition lone poses conceptul nd methodologicl chllenge. Although theory provides very cler prediction, lrge-scle mnipultions under field conditions re needed to mimic ll possile cues for mternl environmentl qulity. This is ecuse, unlike models of si competition, the cue for competitive conditions in the following yer cnnot e relted to the size nd fecundity of the mother plnt which my vry with locl conditions. Insted, the size nd fecundity of ll plnts in the mternl environment re indictive of the potentil numer of neighours in the following yer. Indeed, erlier studies show tht relile cue for productive yer my e closely relted to neighour density or productivity in the previous yer (Pltenkmp & Shw 1993; Crone 1997). This is lso supported y the ide tht if mternl nd offspring environments re similr, mternl environment effects re dptive (see review y Gllowy 2005). Becuse potentil cues for environmentl qulity re difficult to seprte experimentlly, one should idelly mnipulte the entire plnt community in the field. Here, we were le to utilize field experiment in two different climtic regions, where nnul rinfll hs een mnipulted to test whether (prospective) generl competition is importnt in determining offspring germintion. It is importnt to demonstrte the existence of such reltionship, ecuse this my indicte simple ut effective mechnism y which seeds cn prtly predict the future qulity of their environment despite its pprently unpredictle chrcter. In this study, we present the first experimentl test for such mechnism. To test for the generlity of mternl environment effects on germintion, we performed the experiments under conditions tht differed in the importnce of competition for plnt performnce. Nmely, we selected two sites tht differ mrkedly in climte nd competition intensity nd importnce nd three coexisting species tht differ in their competitive response. We predicted tht: (i) offspring germintion frction is negtively correlted with mternl environmentl qulity. As we ssume tht competition is the ultimte reson for the existence of such mternl environment effects, we further hypothesized tht (ii) the negtive reltionship would e more pronounced in sites with high competition intensity nd for less competitive species. Mterils nd methods FIELD RAINFALL MANIPULATIONS The study ws conducted t two sites in trnsition zone etween rid nd mesic climtic regions in Isrel. In the following, we refer to the sites s semi-rid (300 mm men nnul rinfll, Isreli Meteorologicl Service) nd Mediterrnen (540 mm men nnul rinfll), respectively. The semi-rid site is locted 20 km north of Beer Shev in the northern Negev desert, nd the Mediterrnen site is Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

3 1218 K. Tielo rger & M. Petru 15 km southwest of Jeruslem. Both sites re situted on south-fcing slopes nd hve the sme clcreous edrock. The vegettion t oth sites is open shrulnd dominted y Srcopoterium spinosum nd y Thymele hirsut nd Clicotome villos in the semi-rid nd the Mediterrnen sites, respectively (species nmes fter Feinrun- Dothn & Dnin 1991). At the semi-rid site, nnuls my rech 15% cover nd often grow under the cnopy of shrus. At the Mediterrnen site, nnuls ttin up to 60% cover in the open ptches etween shrus (Holzpfel et l. 2006). The sites were suited to test our two hypotheses ecuse competition differs considerly, with neutrl or positive interctions t the semi-rid site nd predominntly competitive interctions t the Mediterrnen site (Holzpfel et l. 2006; Schiffers & Tielörger 2006). Rinfll t oth sites ws mnipulted during two consecutive growing sesons (c. Novemer April), nd Nturlly occurring rinfll ws reduced in dry plots y mnully closing roofs of stndrd PVC rinout shelters constructed 1 m oveground surfce during trgeted rin showers. Following the sme rinfll events, the wet plots were irrigted y drizzle sprinklers instlled t 50 cm ove the ground. Plots with unmnipulted rinfll re referred to s control plots. There were five rndomly locted plots of m for ech of the three rinfll tretments (dry, control, wet) t ech site. Mnipultions continued until rinfll ws reduced or incresed y 30% of the long-term verge nnul rinfll t the sites. Rinfll ws not mnipulted during seed set nd dispersl. The rinfll mnipultions were effective in oth yers. In the first seson ( ), totl rinfll exceeded the long-term verge t oth sites y 144% t the semi-rid site nd 156% t the Mediterrnen site. The rinfll mnipultions chnged totl rinfll mounts to 83% nd 113% of the current rinfll t the semi-rid site, nd to 74% nd 119% t the Mediterrnen site, respectively (Fig. 1). The following seson ( ) ws drier with 89% of the long-term verge t the semi-rid site nd 81% t the Mediterrnen site. In this seson, the rinfll mnipultions reduced nd incresed the current rinfll mounts to 58% nd 134% t the semi-rid, nd 68% nd 141% t the Mediterrnen site, respectively (Fig. 1). It is importnt to note tht rinfll vries unpredictly oth within yers, ecuse the lrge rin systems do not rech the study re t the eginning of the riny sesons (Avid, Kutiel & Lvee 2004, 2009), nd rinfll lso vries unpredictly etween yers (Zhng et l. 2005). Thus, neither the rinfll in the previous yer nor the first rinfll tht triggers germintion in yer is good predictor of the qulity of the coming growing seson. Therefore, there should e strong selection pressure on the trits tht give rise to prediction in the qulity of the environment into which seed germintes, fulfilling requirement of our hypothesis. For illustrting the inherent unpredictility of rinfll t our field sites, we used dt on plnt emergence, survivl nd growth in permnent qudrts, nd in situ rinfll mesurements over 6 yers ( , no mesurements in ). The plnt dt provided: (i) verge iomss per unit re s proxy for yer qulity, nd (ii) n estimte for the mount of rinfll tht triggered the mjor germintion event. Correlting the mount of effective rinfll with verge iomss per unit re yielded non-significnt results for oth sites (semi-rid: r = 0.21, Mediterrnen: r =0.46). STUDY SPECIES We studied three ntive winter nnuls with wide distriution cross Isrel (Feinrun-Dothn & Dnin 1991), high undnce t oth study sites, nd differences in seed dormncy strtegy. Bromus fscicultus (L.) is grss with low dormncy. Biscutell didym (L.) is crucifer with intermedite seed dormncy. Hymenocrpos circinntus (L.) Svi is legume with pods contining two seeds with high dormncy. The species lso differ in competitive response ility nd re thus likely to differ in their response to mternl environmentl qulity (hypothesis 2). Hymenocrpos circinntus is the strongest competitor nd B. didym nd B. fscicultus re wek competitors (Schiffers & Tielörger 2006; C. Ariz & K. Tielörger, unpul. dt). () 1000 Totl rinfll (mm) Semi-rid Dry Control Wet () Mediterrnen (c) Plnt iomss (g) (d) Fig. 1. Totl rinfll (), () nd men (±SE) community iomss of plnts per cm (c), (d) estlished under different mternl environments (dry, control nd wet) in ( first genertion ) nd ( second genertion ). Biomss vlues with similr letters do not differ from ech other (one-tiled t-tests corrected for flse discovery rte). Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

4 Mternl environment effects on germintion 1219 ESTIMATING ENVIRONMENTAL QUALITY Community iomss ws used s the min predictor of the environmentl qulity experienced y the mother plnt nd of the potentil density of competitors in the following seson. This proxy is est suited for testing our min hypothesis ecuse it indictes the productivity of the environment, nd ecuse it is likely to correlte with seed production per unit re. For exmple, we hve found positive correltion etween ove-ground iomss nd fecundity for c. 50 species in the study sites (W. Siewert & K. Tielörger, unpul. dt). It should e noted tht we did not use totl nnul rinfll s n indictor of mternl environment qulity, ecuse the fvourility of seson is lso determined y the within-yer distriution of rin nd not only y its totl. This ws lso supported y correltion nlyses for long-term dt for our sttions (correltions etween rinfll nd iomss: Mediterrnen: r = 0.83, P < 0.05; semi-rid: r = 0.62, NS). Figure 1 confirms this ssumption in tht the tretments did ffect iomss, ut higher totl rin ws not consistently correlted with iomss. Specificlly, the irrigtion mrkedly incresed iomss, ut the dry tretment hd no effect. Community iomss dt were otined from prllel study, where ove-ground iomss ws hrvested nnully t pek seson from five rndomly locted cm qudrts per plot ( totl of 25 per tretment nd site, J. Kigel & I. Konsens, unpul. dt). Biomss ws hrvested ech yer nd in ech mternl environment. DIASPORE COLLECTION AND STORAGE Dispore collection nd hndling followed protocol from previous studies (Petrů et l. 2006; Petru &Tielörger 2008), sed on the need of desert nnul seeds to experience high tempertures to rek summer dormncy (e.g. Boeken et l. 2004). We collected ripe dispores from the tretments in oth sesons, t the time of seed set nd dispersl (April My). Seeds were collected over 4 5 different dys during the fruiting period y crefully scnning the entire re within tretment for ripe seeds nd collecting no more thn three seeds per plnt to minimize the impct on the sites. Dispores from the first seson re referred to s first seed genertion. In the second seson, plnts were collected t distnce of t lest 2 m from the plot s edge (men dispersl distnces of most nnul species re in the rnge of few centimetres, Siewert 2008), to ensure tht collections included only dispores of plnts estlished from seeds produced within the tretment plots. Therefore, this second seed genertion experienced two consecutive sesons of rinfll tretments. For nturlly reking summer dormncy, we stored the dispores collected in ech seson in their originl sites over the summer in gs mde of orgnz (permele trnsprent synthetic fric), ttched to the ground surfce. Ech seson in Septemer, we collected the gs from the field, trnsferred them to lortory for seed counting into equl portions nd immeditely sowed them into n environmentlly controlled germintion experiment. SEED VIABILITY TESTING Seeds tht re stored in the field over summer for dormncy reking my lose their viility. Also, seeds produced under different conditions could differ in their viility, which would ffect germintion frctions. For exmple, seeds produced under wet conditions my e more prone to fungl ttck nd thus e less vile. Seeds produced in d conditions could lso e less vile ecuse of lck of resources. We exmined the viility of five times 20 seeds per species, site nd tretment, y germinting them under lortory conditions (23 C) for 10 dys nd susequently poking ungerminted seeds to exmine whether the emryos were fleshy nd vile (see Pke & Venle 1996). The three species hd high viility in oth sites nd sesons with no significnt vrition mong the mternl environments (B. didym 81 91%, B. fscicultus 62 96%, H. circinntus %). CONTROLLED GERMINATION TRIALS To void confounding with numerous fctors tht control germintion in the field (e.g. soil type, neighour conditions, on-site rinfll; see Petru & Tielörger 2008), we crried out germintion trils in growth chmer (further Phytotron ) t the Herew University in Rehovot, Isrel, in mid-novemer ech seson, for ech species seprtely. We dded 20 B. didym seeds, 40 nd 30 B. fscicultus (in the first nd second seson, respectively) or 40 H. circinntus seeds (20 fruits; ech enclosing 2 seeds) to pots mesuring 12 cm in dimeter nd 12 cm in depth, filled with vermiculite nd soked with tp wter with no dded nutrients. To prevent desicction, we covered the seeds with 1-cm lyer of well-moistened vermiculite. We exposed the seeds to temperture rnge of 16 C dy 10 C night nd wtered them excessively twice dy. In ech seson, the experimentl design (2 sites 3 species 3 mternl environments) hd 20 replictes, resulting in totl of 360 pots. The first seedlings emerged 1 week fter initition of the experiment. Susequently, we counted seedlings every other dy nd removed them from the pots. The experiment ws completed in 4 weeks, when no dditionl seedlings emerged. Results from prllel experiments (Eerhrt 2006) nd viility tests indicted tht most seeds (90 100%) tht did not germinte in the first seson were dormnt nd not ded. DATA ANALYSES To directly test for the predicted site tretment nd species tretment interctions on germintion (hypothesis 2), we performed novs. In these tests, the proportion of offspring seeds germinting per smple ws evluted for the rinfll tretments, species nd sites in full fctoril design (2 sites 3 species 3 rinfll tretments). We tested effects of the rinfll tretments on the second seed genertion in seprte novs, ecuse the second seson ws not true repliction of the first seson s experiment. Nmely, seeds produced in the first seson experienced one seson of rinfll mnipultion, while seeds produced in the second seson cme from plnts whose mothers hd lredy experienced mnipulted seson. The nov model for germintion ws the sme for oth genertions. Germintion dt from oth sesons did not require trnsformtion. Tukey s multiple rnge post hoc tests (P < 0.05) evluted pirwise differences etween rinfll tretments within species nd sites. While the novs tested for the sttisticl interctions, we lso predicted specific negtive effect of mternl environmentl qulity on offspring germintion. Averge iomss of nnuls indictes mternl environmentl qulity nd potentil neighour density in the next yer. We then tested for the predicted negtive reltionship etween verge iomss per tretment nd verge offspring germintion frction (hypothesis 1), using liner regressions. The hypothesized sttisticl interctions were then otined from the ove novs. We corrected for flse discovery rte with the procedure of Benjmini & Hocherg (1995), which hs recently een dvocted for ecologicl studies (Verhoeven, Simonsen & McIntyre 2005). Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

5 1220 K. Tielo rger & M. Petru Results ANALYSES OF VARIANCE AND MULTIPLE TESTS Germintion in the first seson differed significntly etween sites (Tle 1) with higher verge germintion for seeds from the Mediterrnen site (Fig. 2). Differences mong rinfll tretments were significnt for the Mediterrnen site nd non-significnt for the semi-rid site (significnt interction site rinfll tretment, Tle 1; Fig. 2). For two species (B. didym, B. fscicultus) from the Mediterrnen site, germintion frctions were significntly greter for the dry Tle 1. Results of novs for proportionl offspring germintion (G) for 2 yers, two sites (semi-rid nd Mediterrnen), three species (Biscutell didym, Bromus fscicultus nd Hymenocrpos circinntus) nd three rinfll tretments (dry, control nd wet) d.f. G G F P F P Site < <0.001 Species < <0.001 Rinfll tretment < Site species < <0.001 Site rinfll tretment < <0.001 Species rinfll < <0.001 tretment Site species rinfll tretment < <0.001 tretment thn for the control, nd germintion for controls ws greter thn for the wet tretment, while germintion of H. circinntus did not differ etween tretments (Fig. 2,; Tle 1: significnt two-wy nd three-wy interctions etween site, species nd rinfll tretment). Averge germintion in the second seson ws higher for seeds from the semirid site (Fig. 2c). The site nd species effects s well s ll interctions were significnt (Tle 1), indicting speciesspecific nd site-specific responses to the rinfll tretments. Nmely, seeds of B. didym from the wet tretment hd lower germintion (Fig. 2d) thn those from the two drier tretments for the Mediterrnen site, while germintion of B. fscicultus nd H. circinntus differed significntly etween sttions nd tretments ut did not show ny consistent pttern cross sites nd tretments (Fig. 2c,d). REGRESSION ANALYSES The regression nlyses using iomss s predictor for offspring germintion confirmed the findings of the novs. Eight regressions showed negtive slope ut this ws significnt only in four cses. Nmely, iomss in the Mediterrnen site ws negtively correlted with germintion frctions of B. didym in oth yers, for B. fscicultus in the first yer, nd for H. circinntus in the second yer (Tle 2). There ws no significnt negtive correltion for ny species in the semi-rid site. A (significnt) positive slope etween iomss nd germintion ws detected in two cses (H. circinntus Mediterrnen first genertion, B. fscicultus Mediterrnen second genertion). () Offspring germintion (Avg ± 1 SE) Bis Semi-rid () Mediterrnen c c Bro Hym Bis Bro Dry Control Wet Hym (c) Offspring germintion (Avg ± 1 SE) Bis (d) Bro Hym 0.0 Bis Bro c Hym Fig. 2. Men proportionl germintion of seeds collected in (, ) nd (c, d) from different mternl environments (dry, control nd wet) t semi-rid (, c) nd Mediterrnen (, d) site. Seeds were germinted under controlled conditions in the following seson. Different letters ove error rs indicte significnt pirwise differences etween mternl environments within species nd site (Tukey s multiple rnge tests, P < 0.05). Biscutell didym (= Bis), Bromus fscicultus (= Bro) nd Hymenocrpos circinntus (= Hym). Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

6 Mternl environment effects on germintion 1221 Tle 2. Results of regression nlyses (r 2 ) testing in two sites, 2 yers nd for three species Biscutell didym, Bromus fscicultus nd Hymenocrpos circinntus, for negtive reltionship etween verge iomss per unit re nd offspring germintion frction (G) Biomss semi-rid Biomss Mediterrnen Biomss semi-rid Biomss Mediterrnen Discussion G B. didym B. fscicultus H. circinntus * 0.68* 0.10* * 0.21* 0.36* Asterisks indicte significnt results (P < 0.05) fter correction for flse discovery rte. Bold vlues indicte negtive slopes consistent with the predicted reltionship. Our findings suggest tht seed dormncy in nnul plnts inhiting unpredictly vrying hitts my e ffected y the qulity of the mternl environment. However, this predicted negtive correltion etween mternl environmentl qulity nd offspring germintion ws not consistent mong species nd environments. In the following, we discuss first the supporting evidence for our min prediction nd then suggest explntions for the cses tht did not confirm our first hypothesis. In line with our initil hypotheses, the negtive correltion etween mternl environment qulity nd offspring germintion ws only oserved in environments with high competition intensity (e.g. Schiffers & Tielo rger 2006) nd ws stronger for competitively inferior species. Biscutell didym from the Mediterrnen site exhiited consistently negtive reltionship etween rinfll in the seson of seed set nd offspring germintion, nd the two other species showed this pttern in one of the yers. This is the first empiricl evidence for such effects from field-mnipulted popultions of plnts. Therefore, our results represent first experimentl support for the theoreticlly predicted pttern of environmentl mternl effects on germintion (Tielo rger & Vllerini 2005). Bsed on this model, we suggest tht the pttern oserved here is dptive, nd tht it is the result of selective constrints induced y generlized competition fter fvourle sesons. This simple mechnism llows seeds to respond to their future competitive environment long efore germintion. Our findings thus corroorte models out predictive germintion (Cohen 1967; Venle & Lwlor 1980; Ellner 1985), which indicte tht fitness is mximized when the germintion frction is correlted with n environmentl cue tht relily indictes the fvourility of the next seson. The few ttempts to demonstrte such mechnism in nture hve encountered the difficulty of relting n iotic cue (e.g. first rinfll of seson) to the qulity of the coming yer (ut see Pke & Venle 1996). Becuse this correltion does not exist in mny environments, including ours, the lterntive cue we suggest here could e very importnt. Unlike the first rinfll of the seson, the mternl environment is highly relile signl for environmentl conditions (here: neighour densities) in the following seson. This indictes tht diffuse competition my e strong selective force for determining predictive germintion. Besides the supporting evidence, there were severl devitions from the predicted optiml ehviour. We suggest tht these my e explined y the fct tht negtive density dependence (diffuse competition) is the ultimte reson for the evolution of negtive reltionship etween mternl environmentl qulity nd offspring germintion frction (Tielo rger & Vllerini 2005). Such effects should e more detectle in more productive environments nd environments where competition intensity is high. Our study supports this suggestion y finding the effects of mternl environment only t the Mediterrnen site. Recent investigtions t our study sites showed tht indeed, competition etween plnts t the Mediterrnen site is lwys intense, while fcilittion domintes in dry sesons t the semi-rid site nd lnces negtive interctions in wet yers (Holzpfel et l. 2006; Schiffers & Tielo rger 2006). Thelckofevidenceinthesemi-ridenvironmentlsoindictes tht the pttern we detected is unlikely to result from non-dptive effects (e.g. differences in nutrient content of seeds from different tretments) on seed germintion. Another interesting devition from our prediction is tht H. circinntus nd B. fscicultus did not exhiit consistent response to the rinfll tretments. Similr to the differences etween sites, such species-specific ptterns could lso e prtly explined y the role of competition. Seeds of H. circinntus re mong the lrgest within our plnt communities, nd previous experiments hve indicted tht this species is superior competitor (Schiffers & Tielo rger 2006; C. Ariz & K. Tielo rger, unpul. dt). Therefore, competition is less importnt selective force for this species nd mternl environment effects should e less likely to occur. Another, more specultive, explntion for the lck of consistent evidence in B. fscicultus nd H. circinntus my e relted to the generl germintion strtegy exhiited y legumes nd grsses. In our system, legumes hve thick seed cot nd very high dormncy, while grsses usully hve consistently low dormncy, i.e. high germintion (Kigel & Glili 1995; Petru & Tielo rger 2008). This my mke germintion frctions reltively invrile nd result in rther smll responses of germintion to externl cues. Overll, the species-specific ptterns we detected indicte tht the mechnism for predictive germintion we propose here my not e importnt on community level. Therefore, multi-species studies should e performed to test models of optiml germintion (e.g. Venle 2007). It should e emphsized tht unlike previous empiricl nd theoreticl studies, we were serching for effects of the mternl environment t the popultion level. These effects re the result of generlized or diffuse competition s opposed to the so-clled si-competition hypothesis. The si-competition Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

7 1222 K. Tielo rger & M. Petru hypothesis predicts tht seeds of lrge fmilies re selected to hve lower germintion rtes due to the detrimentl effects of siling competition on prentl fitness (Westoy 1981; Ellner 1986; Nilsson et l. 1994; Koyshi & Ymmur 2000). The test of this hypothesis involves collecting siling seeds from mother plnts of different fecundity within popultion nd seson nd mesuring their germintion frctions (Zmmit & Zedler 1990; Hytt & Evns 1998). The uthors of these nd similr study (Philippi 1993) suggested tht informtion out the qulity of the mternl seson my e trnsferred to the offspring vi mternl effects (Roch & Wulff 1987). An indiction of the occurrence of such individul mternl effects could e negtive correltion etween mternl seed production nd offspring germintion. Although our design did not im t testing the si-competition hypothesis, we lso looked t verge fecundity per study species s predictor of offspring germintion. Compred to mesures of generl competition such s rinfll or productivity, mternl fecundity ws reltively poor predictor of offspring germintion, with only one significnt negtive correltion (see Appendix S1 in Supporting Informtion). This oservtion lso finds support in prllel study tht hs directly tested, nd filed to support, the si-competition hypothesis for our three focl species (Eerhrt 2006). We therefore suggest tht individul mternl effects re unlikely to determine the pttern detected here. Yet, studies re needed tht re explicitly designed to differentite etween our new hypothesis nd the si-competition hypothesis. A recent study showed tht the phytochrome system my e involved in germintion responses to sesonl cues, including mternl effects on germintion (Donohue et l. 2007). Thus, n lterntive wy of detecting the fvourility of seson independent of individul mternl performnce my e vi high densities of plnts round the mother (Pltenkmp & Shw 1993; Crone 1997) utilizing different red : fr red rtios. Indeed, we found negtive reltionships etween site productivity in the yer of seed production nd offspring germintion. Productivity should correlte with undnce of neighours, nd this my e n even etter cue for predicting overcrowding thn mternl fecundity ecuse it is not ffected y chnce effects on the individul mother plnt. Also, such mechnism would llow prediction of the potentil intensity of generlized competition (s modelled y Tielo rger & Vllerini 2005), independent of the density of silings. Clerly, the mechnisms ehind the ptterns oserved here merit more ttention in physiologicl studies on seed dormncy. In summry, our findings suggest tht there my e simple ut effective mechnism llowing seeds to predict their future success y utilizing informtion out the environment of their mother. However, the reltive importnce of this mechnism proly depends on whether or not competition is strong selective force nd whether or not there is strong selection on seed dormncy. Becuse our study is the first of its kind, we cll for further experiments testing the generlity of the theoreticlly predicted ehviour nd the species- nd site-specific ptterns oserved here. Acknowledgements We pprecite prcticl support y M. Sternerg nd J. Kigel nd y the stff of the Phytotron t the Agriculturl Fculty of the Herew University in Rehovot nd y C. Ariz, Y. Vortmn, C. Holzpfel, A. Hriton, T. Petrusková, Y. Mutsfi nd H. Prg. The provision of iomss dt y J. Kigel is grtefully cknowledged. D. Cohen, K. Donohue, R. Kdmon, M. Seifn, A. Vllerini, the Hndling Editor, nd three nonymous referees provided vlule comments on nerlier drft. Weregrtefulforcrefulproof-redingnd lnguge editing y M. Bilton. This study is prt of the GLOWA Jordn River project funded y the Germn Federl Ministry of Eduction nd Reserch (BMBF). References Avid, Y., Kutiel, H. & Lvee, H. (2004) Anlysis of eginning, end, nd length of the riny seson long Mediterrnen rid climte trnsect for geomorphic purposes. Journl of Arid Environments, 59, Avid, Y., Kutiel, H. & Lvee, H. (2009) Vrition of Dry Dys Since Lst Rin (DDSLR) s mesure of dryness long Mediterrnen Arid trnsect. Journl of Arid Environments, 73, Benjmini, Y. & Hocherg, Y. (1995) Controlling the flse discovery rte: prcticl nd powerful pproch to multiple testing. Journl of the Royl Sttisticl Society B, 57, Boeken, B., Ariz, C., Guttermn, Y. & Zdy, E. (2004) Environmentl fctors ffecting dispersl, germintion nd distriution of Stip cpensis in the Negev Desert, Isrel. Ecologicl Reserch, 19, Bulmer, M.G. (1984) Delyed germintion of seeds: Cohen s model revisited. Theoreticl Popultion Biology, 26, Cluss, M.J. & Venle, D.L. (2000) Seed germintion in desert nnuls: n empiricl test of dptive et hedging. Americn Nturlist, 155, Cohen, D. (1966) Optimizing reproduction in rndomly vrying environment. Journl of Theoreticl Biology, 12, Cohen, D. (1967) Optimizing reproduction in rndomly vrying environment when correltionmyexist etweentheconditions tthetime choicehs to emdendthesusequentoutcome. JournlofTheoreticlBiology, 16, Crone, E.E. (1997) Prentl environment effects nd cyclicl dynmics in plnt popultions. Americn Nturlist, 150, Donohue, K., Heschel, M.S., Ching, G.C.K., Butler, C.M. & Bru, D. (2007) Phytochrome medites germintion responses to multiple cues. Plnt, Cell nd Environment, 30, Eerhrt, A. (2006) Do silings void ech other? An empiricl test of the siling competition hypothesis long steep climtic grdient. Diplom Thesis, University of Tüingen, Tüingen, Germny. Ellner, S. (1985) ESS germintion strtegies in rndomly vrying environments. I. Logistic type models. Theoreticl Popultion Biology, 28, Ellner, S.(1985)ESSgermintion strtegies inrndomlyvryingenvironments. II.Reciprocl yield-lwmodels.theoreticlpopultionbiology, 28, Ellner, S. (1986) Germintion dimorphisms nd prent-offspring conflict in seed germintion. Theoreticl Popultion Biology, 123, Ellner, S. (1987) Competition nd dormncy: renlysis nd review. Americn Nturlist, 130, Feinrun-Dothn, N. & Dnin, A. (1991) Anlyticl Flor or Eretz-Isrel. Cn Pulishing House Ltd., Jeruslem. Gllowy, L.F. (2005) Mternl effects provide phenotypic dpttion to locl environmentl conditions. New Phytologist, 166, Holzpfel, C., Tielo rger, K., Prg, H.A., Kigel, J. & Sternerg, M. (2006) Annul plnt-shru interctions long n ridity grdient. Bsic nd Applied Ecology, 7, Hytt, L.A. & Evns, A.S. (1998) Is decresed germintion frction ssocited with risk of siling competition? Oikos, 83, Kigel, J. & Glili, G. (1995) Seed Development nd Germintion. Dekker, New York. Koyshi, Y. & Ymmur, N. (2000) Evolution of seed dormncy due to si competition: effect of dispersl nd inreeding. Journl of Theoreticl Biology, 202, Léon, J.A. (1985) Germintion strtegies. Evolution. Essys in Honour of John Mynrd Smith (eds P.J. Greenwood, P.H. Hrvey & M. Sltkin), pp Cmridge University Press, London. Nilsson, P., Fgerström, T., Tuomi, J. & A ström, M. (1994) Does seed dormncy enefit the mother plnt y reducing si competition? Evolutionry Ecology, 8, Pke, C.E. & Venle, D.L. (1996) Seed nks in desert nnuls: implictions for persistence nd coexistence in vrile environments. Ecology, 77, Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,

8 Mternl environment effects on germintion 1223 Petru, M. & Tielörger, K. (2008) Germintion ehviour of nnul plnts under chnging climtic conditions: seprting locl nd regionl environmentl effects. Oecologi, 155, Petru, M., Tielo rger, K., Belkin, R., Sternerg, M. & Jeltsch, F. (2006) Life history vrition in n nnul plnt under two opposing environmentl constrints long n ridity grdient. Ecogrphy, 29,1 9. Philippi, T. (1993) Bet-hedging germintion of desert nnuls: eyond the first yer. Americn Nturlist, 142, Philippi, T. (1993) Bet-hedging germintion of desert nnuls: vrition mong popultions nd mternl effects in Lepidium lsiocrpum. Americn Nturlist, 142, Pltenkmp, G.A.J. & Shw, R.G. (1993) Environmentl nd genetic mternl effects on seed chrcters in Nemophil menziesii. Evolution, 47, Roch, D.A. & Wulff, R.D. (1987) Mternl effects in plnts. Annul Review of Ecology nd Systemtics, 18, Schiffers, K. & Tielo rger, K. (2006) Ontogenetic shifts in interctions mong nnul plnts. Journl of Ecology, 94, Siewert, W. (2008) The dispersl dormncy trde-off in nnul plnts: putting model predictions to the test. Diplom Thesis, University of Tüingen, Tu - ingen, Germny. Tielo rger, K. & Vllerini, A. (2005) Cn seeds predict their future? Germintion strtegies of density-regulted desert nnuls. Oikos, 111, Tuljpurkr, S. & Istock, C. (1993) Environmentl uncertinty nd vrile dipuse. Theoreticl Popultion Biology, 43, Vllerini, A. & Tielörger, K. (2006) Effect of ge on germintion of dormnt seeds. Theoreticl Popultion Biology, 70, 1 9. Venle, D.L. (2007) Bet-hedging in guild of desert nnuls. Ecology, 88, Venle, D.L. & Lwlor, L. (1980) Delyed germintion nd dispersl in desert nnuls: escpe in spce nd time. Oecologi, 46, Verhoeven, K.J.F., Simonsen, K.L. & McIntyre, L.M. (2005) Implementing flse discovery rte control: incresing your power. Oikos, 108, Westoy, M. (1981) How diversified seed germintion ehviour is selected. Americn Nturlist, 118, Zmmit, C. & Zedler, P.H. (1990) Seed yield, seed size, nd germintion ehviour in the nnul Popogyne rmsii. Oecologi, 84, Zhng, X., Aguilr, E., Sensoy, S., Melkonyn, H., Tgiyev, U., Ahmed, N. et l. (2005) Trends in Middle Est climte extreme indices from 1950 to Journl of Geophysicl Reserch, 110, D Received 17 Ferury 2010; ccepted 30 April 2010 Hndling Editor: Michel Hutchings Supporting Informtion Additionl Supporting Informtion my e found in the online version of this rticle: Appendix S1. Evlution of possile effects of mternl fecundity on offspring germintion. As service to our uthors nd reders, this journl provides supporting informtion supplied y the uthors. Such mterils my e re-orgnized for online delivery, ut re not copy-edited or typeset. Technicl support issues rising from supporting informtion (other thn missing files) should e ddressed to the uthors. Ó 2010 The Authors. Journl compiltion Ó 2010 British Ecologicl Society, Journl of Ecology, 98,