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ECOPHYSIOLOGY OF SEED GERMINATION ÉÍPINUS HALEPENSIS AND Ñ. BRUTIA

Costas Á. ThanosDepartment ÏÉ Botany, Faculty ÏÉ Biology, University ÏÉ Athens, Panepistimiopolis,Athens 15784, Greece. E-mail: cthanos@biology.db.uoa.gr

Introduction

Aleppo and the east Mediteuanean (or brutia) pines (Pinus halepensis and Ñ. bru-tia, respectively) are obligate seeders; therefore, the regeneration ofboth these twospecies and oftheir pine forests is totally dependent õñïç seedling recruitment (par-ticularly ßç post-fire conditions; Thanos 1999). Every year, mature pine trees pro-duce prolific numbers of seeds, a large fraction of which remain enclosed withintheir cones (canopy seed bank) and maintain their viability for long ÑeÞïds (Cucuiet áÉ. 1996, Daskalakou and Thanos 1996).

Éç their discourse ïç serotiny (mostly for Southem Hemisphere plants), Lamontet áÉ. (1991) put forth (and discussed) 9 adaptive postulates. Five ofthese adaptivecharacteÞstics may be applicable to the Mediteuanean pines: 1. Protection of seeds(from both consumers and fire). 2. Maximisation of seed availability after a fire. 3.Efficient and homogeneous, post-fire, wind seed dispersal. 4. Minimisation ofpost-dispersal hazards (seed colour mimicry and elimination or reduction of predatorpopulations). 5. Optimisation of seed germination and early seedling growth sub-strate (nutrients added by fire and considerably decreased competition for light andwater). Éç regard to the latter, water and light seem to be most important, as pinesare generally well adapted to nutrient poor soils (Mirov 1967). Hanley and Fenner(1997), working with seedlings of Ñ. brutia over the first 12 weeks of growth,showed that deÑÞvatiïç of any single macronutrient had çï effect ïç growth.

Éç addition to the above, the character of partial cone serotiny (or seed brady-chory, Thanos 1999), shared by both Ñ. halepensis and Ñ. brutia (Daskalakou andThanos 1996), confers a dual strategy of regeneration. Besides the en masse post-fire germination, their seeds can exploit and colonise open and disturbed areas vir-tually every year, also in fire-free conditions.

Seed Morphology

Despite their close phylogenetic relationship, seeds of Ñ. halepensis and Ñ. brutiashow marked differences ßç both their structure and, as will be discussed ßç the nextsection, germination behaviour.

Ecology, Biogeográphy ánd Mánágement ÏÉ Pinus hálepensisand Ñ brutia Forest Ecosystems in the Mediterráneán Basin, ññ. 37-50edited by G. Ne'emán ánd L. Trábáud(ò) 2000 Báckhuys Publishers, Leiden, The Netherlánds

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38 C.A. Thános

Firstly, the average seed weight is significantly higher in brutia than in Aleppo pine,eog., Nahal (1983) refers to a gross average seed weight of 50 mg for R brutia asopposed to 15-20 mg for R halepensis. In an extensive survey of 50 Turkish provenanc-es of R brutia seeds, Sefik (1965) determined an average seed weight of 56 mg (range38-68 mg); Isik (1986) found a higher average (63.8 mg) from 6 Turkish provenanceswhereas Panetsos (1981) reported a considerably lower value from various Greekprovenances (40.5 mg). Similarly, Aleppo pine seed weight has been found to varywidelyamong collections (12-30 mg) according to several sources (eog., Debazac andTomassone 1965, Pelizzo and Tocci 1978, and Thanos et áÉ. 1995). Figure 1 shows thelinear regression curves between average seed weight and average number of cotyle-dons in numerous accessions ofboth specieso The grand average values for seed weightare 20 mg for R halepensis and 51 mg for R brutia and there is minimal overlapbetween the ranges of values. The grand average number of cotyledons are 7.4 and 8.4,respectively; a considerably steeper slope is obtained in Aleppo pine than ßç brutia.

Seed weight has been shown to vary among locations and altitudes; comparingvaÞïus Italian provenances of R halepensis, Cuccui et áÉ. (1996) found positive andstatistically significant conelation coefficients between site altitude, ïç the onehand, and seed weight and germinability, ïç the other. Mean seed weight of R bru-(ßá was considerably more variable among trees than within a tree, and it was almostconstant within a single cone (Thanos and Daskalakou 1993). Finally, seed weightmay conelate positively with tree and cone size; ßç a nursery study (ÌatÆßÞs 1998),the cones produced by 10-year-old Aleppo pine saplings showed particularly highvalues of cone and seed weights (2807 mg), which were attributed to the favourablegrowing conditions.

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Fig. 3. Final dark germination as a function oftemperature in Pinus háZepensis (Á) and Ñ. brutiá (Â).Each curve conesponds 10 a different, Greek seed provenance: 7 for Aleppo pine and 3 for brutia;1: Lasithi (eastem Crete), 2: Thasos Island (Aegean Sea), and 3: Soufli (northem Greece): Verticallines represent S.E. (After Thanos et áÉ. 1995 and Skordilis and Thanos 1995).

Temperature Range ï/ Germination

Magini (1955) studied germination as a function oftemperature and placed the opti-mum for Ñ. halepensis seeds at 18.5°C; high and low temperatures (25-28°C andbelow 10°C) retarded or inhibited germßçation. In an extensive survey of 50 Turkishprovenances of Ñ. brutia seeds, Sefik (1965) determined an average germßçabilityof 78% at 20°C. ~

Several studies with Greek provenances confirmed the optimum temperaturerange (15-20°C) for Aleppo pßçe seed germination ßn darkness (Thanos andSkordilis 1987, Skordilis 1992, Skordilis and Thanos 1995). Figure 3Á, ßç additionto the optimal range (15- 20°C), illustrates the suboptimal cool temperatures (around10°C) and the 'ambiguous' extremes 5 and 25°C. Thus a particular provenance maygerminate fully at on1y a single end ofthe temperature range (e.g., provenances 5and 7) whereas other provenances follow a less clear pattem. Calamassi et áÉ. (1984)

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'9'. Ecophysiology ÏÉ seed germinátion in Pinus hálepensis ánd Ñ. brutiá 41

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studied the effects oftemperature ïç 9 circum-Mediterranean provenances and con-cluded that dark germination is optimal ßç the range 15-21°C (average means 82-83%); at 24°C germination is considerably decreased to a gross average of 58%.

Á similar optimal temperature range (15-20°C) has been repeatedly observed forÑ. brutia seeds (Sefik 1965, Isik 1986, Thanos and Skordilis 1987, Skordilis 1992).Nevertheless, ßç several provenances ofthis species a more or less pronounced dor-mancy has been observed. Figure 3Â illustrates germinability as a function oftem-perature ßç three representative 10ts of brutia pine seed.

Rate ÏÉ Germination

Calamassi et áÉ. (1984), working ïç 9 cßrcum-ÌedßteðaneanÑrïveçances of Aleppopine, found a slow pace of dark germination; overall average Ô 50 values (time need-ed for 50% of final germination) were 12,9.5 and 10 days at the optimal tempera-tures of 15, 18 and 21°C, respectively. Á similarly 'sluggish' germinability was alsoobserved ßç several additional cases with both pine species (Thanos and Skordilis1987, Skordilis1992, Skordilis andThanos 1995). This 'delay' mechanism ofseedgermination in these pines (and numerous other Ìediteðaçean plants) is stillunknown; however, it shou1d not be attributed to a seed-coat-imposed, restrainingeffect because decoating ßç both Aleppo and brutia.. pine seeds resulted in ïçlÕ aslight enhancement of germination rate (Skordilis 1992, Thanos et áÉ. 1995).

Successive applications of Hg2+ and Cl- ions resulted in a dramatic promotionof the germination rate of Aleppo pine seeds; Ô 50 was decreased to ïçlÕ 2 days froma value of 9 days for the untreated seeds (Thalouarn and Heller 1977). This stimu-lation has been attributed to modified water permeability because an early increaseof embryo (plus megagametophyte) imbibition was observed ßç treated seeds fol-10wed by both reserve mobilisation and radicle growth (Pargney and Thalouarn

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Time (days)

Fig. 4. Germination time courses for coasta1 (Pinus hálepensis, Ñ. brutiá) and mountainous (Ñ. syl-vestris, Ñ. nigrá) pine species (a11 seed provenances from Greece) at optima1 conditions (20°C, 12 hwhite 1ight ÑhïtoÑeÞïd) (After Skordilis and Thanos 1997).

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.. ..~42 C.A. Thános1978). A1though the mode of action of Hg2+ ions remains e1usiíe, the presence ofthe seed coat is required for the manifestation of germination induction.

Among the 13 pines be1onging to the assembly of the Ìediteðaçean pines(according to Miroí 1967 and K1aus 1989), Ñ. hálepensis and Ñ. brutiá are placed(ïç an eíolutionary basis ofmorphological characters, K1aus 1989) ßç the group of'Ìedßteðaneaç shore and island pines' (together with Ñ. cánáriensis, Ñ. pineá andÑ. pináster). The remaining species are grouped ßç two distinct classes ofmountain-ous pines (the first ofwhich cïmÑÞses the Diploxylon species). These three class-es seem to conform well with seed germination behaíiour (Skordilis and Thanos1997); ßç particular, the mmtime Ìediteðaçean pines, Ñ. hálepensis and Ñ. brutiá,show a íery slow germination rate whereas the mountainous species germinate con-siderably faster (Fig. 4).

The Effect ÏÉ Light on Germinátion

The role of light and the mediation of the phytochrome photoreceptor system isgenerally well studied ßç pine seeds and has been known for some time (Toole,1973). Neíertheless, and despite the well known photophi1ous nature ofboth spe-cies (Trabaud 1995), until recently ïçlÕ preliminary results by Shafiq (1979a) andCa1amassi (1982) had reíealed an oíerall inductiíe rple of light ïç seed germina-tion of brutia and Aleppo pine, respectiíely. Éç a number of detailed studies ïç thesubject, the physiological and ecological importance of light was iníestigated(Thanos and Skordilis 1987, Skordilis 1992, Skordilisand Thanos 1995, Thanos etáÉ 1995). It was found ßç both species that continuous red (R) light or diurnal whitelight always promotes the germination rate and sometimes the maximum percent-age as well. Continuous or intermittent far-red (FR) light not ïçlÕ inhibits germina-tion ßç both species, but also induces a secondary dormancy; the relief of this pho-todormancy is under phytochrome control as shown by R-FR reíersibility.

Dormáncy ánd Strátificátion

A1eppo pine seeds are generally non-dormant; ïç the other hand, seíeral proíenanc-es of Ñ. brutiá exhibit considerable and íarying degrees of dormancy. Moreoíer, Isik(1986) was able to show that among six populations from different eleíations (south-em Turkey) the high elevation proíenances germinated more slowly and had lowergermination percentages. In another case with three Greek proíenances from con-trasting latitudes, dramatic differences ßç the degree of dormancy were noted (Fig.3Â). Stratification (1-3 months) resulted ßç a considerable promotion of Ñ. brutiá seedgermination (Fig. 5Á). Neíertheless, the inductiíe effect of stratification was shownto differ among the three proíenances, escalating from a simple increase of germina-tion rate (ßç the southem seed lot from Crete) through a broadening of the tempera-ture range of germination (ßç the intermediate lot from Thasos Island) to a dramaticrelease from a particularly deep dormancy (ßç the northem lot from Thrace). Thesedeeply dormant seeds of the latter proíenance displayed an absolute stratificationrequirement; prolonged illumination or seed coat scmfication could on1y slightlysubstitute for the promotiíe effect of pre-chilling. Moreoíer, a considerable interac-tion between far-red light and stratification was reíealed ßç the dormant seeds of Ñ.

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.....Ecophysiology ï/ seed germination in Pinus halepensis and Ñ. brutia 43

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Fig. 5. Á. Final gennination of Pinus brutia seeds (Soufli provenance) at 15°C and darkness, aftervarious durations of a stratification pre-treatment. Control: seeds kept in darkness throughout. FinalFR: seeds given a single 30-min 10ng far-red pulse at the end ofthe chilling pre-treatment. WeeklyFR: seeds given weekly, 30-min 10ng, far-red irradiations throughout pre-chilling. (After Skordilisand Thanos 1995). Â. Time course of Pinus halepensis seed gennination in simulated autumn con-ditions under 3 different light regimes: diurnally alternating far-red (FR) - darkness ("intense",FR1; "mild'" FR2) and continuous darkness (D). The fluctuating lines represent the average dailytemperature at a representative, semi-arid Mediteuanean environment (Athens Airport); time Ï cor-responds to November 8. The seeds were extracted from freshly-matured cones (Ï years old) col-lected from the forest ofVillia, Attica (After Daskalakou and Thanos 1996).

brutia (Fig. 5Á); far-red pu1ses during stratification cou1d either cancel or diminishthe germination promotion induced by low temperatures (Skordilis and Thanos 1995).

Én the survey of 50 Turkish proíenances of Ñ. brutia (Sefik 1965), stratificationwas found to decrease germination rate and increase germinability (aboíe the gross

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44 C.A. Thános

average 78%; this indicates that a few provenances may have been dormant). Inaddition, Shafiq and Omer (1969) found that stratification ßç the sand for 45 daysat 4°C increased the germinability of Ñ. brutia seeds considerably. Similarly, Falusi(1982) found a markedly higher rate of germination ßç stratified seeds of Ñ. brutia.Although the dormancy observed in brutia pine seeds evidently belongs to theembryonic type, there may be some interaction with the seed coat, as implied ßç theprevious paragraph. Shafiq (1970/71) treated Ñ. brutia seeds with dense sulphuricacid and observed a decrease of germinability (obviously as a result of embryodamage) while the mechanical scarification of the seed coat led to a significantlyimproved germination at 25°C (Shafiq 1979b).

Calamassi et á!. (1984) studied the effects of stratification ïç 9 circum-Ìediteðanean provenances of Aleppo pine and an overall suppression of germin-ability was obtained (from a grand mean of 83% for untreated seeds to 77% and 69%after 1 and 2 months respectively). Although not all provenances respond similarly(some are unaffected by stratification), the rate of germination is enhanced (overallmeans ofTso decreased by 5 and 6 days, respectively). Similarly, Skordilis (1992)and Skordilis and Thanos (1995) found that a stratification treatment for longer than1 month resulted in a considerable decrease ßç germinability of Aleppo pine; thisdecline was attributed to a gradual necrosis of embryos in cold temperatures.

..

Moisture Stress, ñÇ and Inhibitors

Germination in both species is gradually suppressed with increasing concentrationsof osmotic solutions (moisture or hydric stress). Nevertheless, the data obtained weregreatly variable not only among provenances but also among researchers (Calamassiet á!. 1980, Fa1usi and Ca1amassi 1982, Fa1usi et á/. 1983, Thanos and Skordilis 1987,Skordilis 1992, Henig-Sever et á/. 1996). According to Thanos and Skordilis (1987),when seeds are osmotically stressed the slow rate of germination becomes even slow-er, although the final germination percentage is inhibited only at a range of very lowosmotic potentials. Ne'eman et á/. (1993) and Henig-Sever et á!. (1996) studied therole of ash and ñÇ ïç seed germination of Aleppo pine and found a considerable sup-pression at values 9-10, similar to those encountered under post-fire conditions ßç thealkaline ashes. Recently, Henig-Sever et á/. (2000) found that this inhibition may becounteracted by an enhancement of seed germination brought forth by nitrate andammonium ions (also known to occur in the soil of a recently burned forest). ÁÂÁwas found to inhibit seed germination ßç Ñ. brutia and its action was reversed by asubsequent application of GA3, whereas kinetin and benzyladenine were ineffective(Kabar 1998). The application of three systemic insecticides was toxic to both seedsand seedlings of A1eppo pine (Olofinboba and Kozlowski 1982).

Protocols ofGermination

Seed germination rules by the Intemational Seed Testing Association, ISTA (1993)include instructions for A1eppo pine, only. They recommend germination at a con-stant temperature of 20°C, first count at 7 - last count at 28 days, with çï further

comments. Similarly, Young and Young (1992) suggest 20°C for 28 days but theyadd a note that seeds are sensitive to warm temperatures. Light is not mentioned and

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.. Ecophysi%gy ÏÉ seed germinátion in Pinus há/epensis ánd Ñ brutiá 45çï suggestions are furnished at all for Ñ. brutia. Ïç the basis of the e×ÑeÞÉçeçtaÉevidence descÞbed previously, it is suggested that germßçation protocols be finallyformulated as follows:- Pinus ha/epensis ÔÑ, 20°C, 7-28 days (first-last count), white light.- Pinus brutia ÔÑ, 20°C, 7-28 days (first-last count), white light; iffinal germina-

tion is below 70-80% repeat the test after a 2-month-long pre-chillßçg treatment.[ÔÑ: ïç top ofpaper]

Ecology of Seed Germination

Éç a speculative but far-reaching discussion, Magini (1955) emphasised the difIer-ence ßç the optimum temperature for seed germination between Aleppo and umbrel-la pßçes (ïç the one hand) and a number of mountainous pines. This difIerence wasattributed to diverging life history adaptations, namely seedling emergence and sur-vival ßç relation to their cïðeSÑïçdßçg, cÞtßcaÉ (res!Þctßve) seasons: dry and hotsummer for the former and frozen winter for the latter. Thus germination is assumedto take place doong fall and wßçter ßç the former and SÑÞçg ßç the latter and Maginishou1d be acknowledged as the pioneer of pßçe seed germination ecology.

As stressed ßç the introduction, post-fire regeçeötßïç of both species dependsexclusively upon the canopy seed bank, due to the short life span of their soil seedbanks and the consumption by fire of all the seeds that happen to be found ßç thesoil (Daskalakou and Thanos 1996). Therefore, considerably 10ng seed 10ngevity isof paramount importance, and indeed it seems that this is the case for both species.Viability of Aleppo pßçe seeds within serotßçous cones was found to decrease at aslow pace with cone age (Cuccui et áÉ. 1996, Daskalakou and Thanos 1996). Éç Ñ.brutia, germination tests showed that seeds remaining ßç closed cones had high ger-mination ability (Eler 1990); moreover, Selik (1958) reported that even nine-year-old cones contain germinable seeds.

Cones confer a noteworthy protection to seeds against the lethal temperatures offire, as shown by several field and laboratory studies. For instance, Trabaud andÏus!Þc (1989) found that high temperatures ßç a simulated fire ßç the lab killed allA1eppo pine seeds. Martinez-Sanchez et á/. (1995) applied short heat treatments toÑ. ha/epensis seeds and concluded that germßçation is suppressed by the tempera-ture ßçcrease that can be reached ßç soils doong a fire. Similarly ßç Ñ. brutia, the ger-mination percentage of the seeds decreased significantly when 'bare' seeds wereexposed to high temperatures from 70-90°C (Neyisci 1988). Seedlßçg survivorshipand growth ßç Ñ. brutia was reduced after the seeds had been exposed to tempera-tures exceeding 90°C (Han1ey and Feççer 1998); with a thermal pre-treatmentabove 110°C, a rapid declßçe ßç germßçation was also observed. Ïç the other hand,when seeds were left inside the cones that were heated to 125°C, the seeds remaßçedviable (Cengiz 1993).

Loisel (1966) studied Aleppo pine seed germßçation ßç the field usßçg a phyto-sociological approach. He sowed pßçe seeds ßç 9 difIerent vegetation associationsand monitored seedling emergence and surviva1. Éç 7 out of 9 vegetation types ger-mßçation was satisfactory whereas significantly 10wer germination levels wereobserved ßç 2 ofthem that were dominated by the grass Brachypodium ramosum.

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Because pine seed germination ßç the field takes place en masse almost exclu-sively ßç post-fire conditions, most ofthe available information deÞves from stud-ies of burned sites (Thanos 1999). Pine seed germination and seedling emergencetake place almost exclusively doong the first post-fire wet season; more specifical-ÉÕ, their occurrence usually takes the form of a massive wave early ßç the ÑeÞïd(October-January), closely following the start of the wet season, as shown by bothfield (Daskalakou 1996) and laboratory studies (Thanos and Skordilis 1987;Skordilis and Thanos 1995). Doong the second post-fire rainy ÑeÞïd çï additionalseed1ings are usual1y observed. Éç Ñ. brutia, it was postu1ated that this pattem maybe modified ßç certain regions with more severe winters; the seed1ing recruitmentprofile is shifted to the late winter or early SÑÞçg months, possibly as a frost-avoid-ing mechanism of the vulnerable seed1ings (Skordilis and Thanos 1995). Thus thedifferences observed ßç the germination behaviour among the vaÞïus Ñ. brutiaprovenances (Fig. 3Â) may be attributed to a variable ecophysiological strategy ßçregard to the temporal pattem of seed1ing emergence and establishment. Accordingto the variants of this strategy, seed germination is timed to occur doong eitherSÑÞçg (ßç regions with relatively cold and moist climates) or autumn and early win-ter (ßç southem, mild and dry areas) or both (ßç intermediate conditions).

The above postulated strategy is based ïç a particular kind of seed dormancy thatcan be manipulated by stratification. Falusi (1982), b~sed ïç a study ofthe stratifi-cation effect ïç seeds of Ñ. brutia from different provenances, was the first to sug-gest differential timing of autumn versus spMg germination ßç relation to seed1ingsurvival during the cÞtßcaÉ winter season. A1though much remains to be done to val-idate this hypothesis, certain field data and observations do support it. Eron (1987)reported that germination of Ñ. brutia generally starts ßç November at lower eleva-tions (250-300 m), ßç February at midd1e elevations (350-650 m) and ßç ÁñÞÉ athigher ones (700-800 m). Ozdemir (1977) found that germination of Ñ. brutia ßç theAntalya region starts ßç mid-January and mid-March at the lower and higher eleva-tions, respectively. In two other cases, an initial small part of the population germi-nated doong the winter months, November to February, and a 'burst' of germinationoccurred ßç March and ÁñÞÉ (Thanos et áÉ 1989, Eler and Senergin 1990).

Because pine seed germination takes place on1y doong the first post-fire wetseason, it is of paramount importance for the survival of the ensuing population thateðatßc germination be reduced or eliminated. Therefore, the slow rate of germina-tion is considered an adaptation to delay germination until well into the wet seasonand ßç this way reliable water availability is ensured.

Å×ÑeÞmeçts under daily altemating conditions of light and temperature resem-bling natural conditions led to the conclusion that field germination is feasiblethroughout the rainy season of the Ìedßteðaneaç-type climate and is stronglyfavoured ßç open, sunny sites (Daskalakou and Thanos 1996). Figure 5 shows thatwhite light ßðadiatßïç doong the warm part of simulated autumnal day results ßç amarked promotion of germination, whereas intense far-red light (simulating a densecanopy cover) causes a significant inhibition, ßç agreement with previous similarresults (Thanos and Skordilis 1987).

Henig-Sever et áÉ (1996) confirmed the relatively high resistance of pine seedgermination towards osmotic stress (previously reported by Thanos and Skordilis1987) and suggested that this may constitute an adaptation to the post-fire, ash-

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Ecophysiology ofseed germination in Pinus halepensis and R brutia 47

eooched (i.e., low osmotic potential) substrates. According to Saracino et á!. (1998),ashes and particularly lipids produced during fire by combustion of various plantmateÞaÉs may affect A1eppo pine seed germination. This postulated effect is attribut-ed to the modified hydrological properties ofthe burned soil and eventually suppress-es seed1ing emergence and affects spatial pattems. Henig-Sever et á!. (1996,2000)concluded that increased ñÇ and substantial concentrations of nitrate and ammonium,in the burned soil, are important factors for seed germination and forest regeneration.

Conclusions and Suggestions for Future Research

Based ïç several vegetative and taxonomic traits, Mirov (1967) and, later, Panetsos(1981) have granted to Ñ. brutia the attribute of 'variable' whereas Ñ. halepensis,despite its postulated close evolutionary relationship to the former and inversely toits large geographical distribution, is considered 'stable'. Depending õñïç the alti-tude and latitude of the provenance, this vaÞabßÉßty of Ñ. brutia is also displayed byseed morphological characters (seed size and seed coat contribution) as well as bythe 'plasticity' of seed germination (degree of dormancy, stratification requirementsand, eventually, timing of seed1ing emergence).

Small seed size ßç Pinus has been cïðelated with.both invasibility (Richardsonet á!. 1990) and fire-resilience (McCune 1988). CïçsßdeÞçg the factors which con-tribute to the invasive potential of exotic pines ßç South African mountain fynbos,,Richardson et á!. (1990) concluded that the most successful species (Ñ. halepensis,Ñ. pinaster and Ñ. radiata) are fire-resilient, have small seeds, low seed-wing load-ing, short juvenile ÑeÞïds, moderate to high degrees of serotiny and are relativelypoor fire-tolerant as adults. ÂÕ examining 33 spp. (34 taxa) of North AmeÞcaçpines, McCune (1988) has descÞbed 5 adaptive modes; his group 4 cïmÑÞses 11fire-resilient spp. (12 taxa) that are precocious reproducers and produce small (andlight) seeds (9.7 mg, the smallest value among the 5 groups), often in serotinouscones (by far the highest value among the 5 groups). Although both A1eppo and bru-tia pine species might be placed ßç the fire-resilient group of McCune (1988) an~the relevant one ofRichardson et á!. (1990), it could be argued that the significant-ÉÕ higher (and extremely plastic among provenances) seed weight of Ñ. brutia andits lower (though not well documented) degree of serotiny might be an indicationfor a rather marginal participation of the latter species ßç the above-mentionedgroups. Moreover, the 'adoption' of an embryonic dormancy relieved by chillingand its postulated association with a 'radiating' seed1ing recruitment strategy mightbe considered as evidence of an evolutionary divergence from dry and fire-pronehabitats (typical of Aleppo pine) towards colder and wetter ones.

Éç conclusion, long-lasting canopy seed banks are formed ßç both species where-as their soil seed banks are transient and rather unimportant. Seed longevity withincones has been found satisfactory, and cone scales protect seeds from the lethal heatof fire. Seeds are dispersed in summer or after a fire and germination takes place ata relatively slow pace and preferably at open, sunlit sites under the cool tempera-tures of autumn that coincide with the onset of the wet season. Exceptions to thisrule are several dormant provenances of Ñ. brutia that may show either an extensiverecruitment pattem cïveÞçg most of the wet season or a SÑÞçg-Ñeaked pattem in

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extremely cold habitats (northernmost latitudes or highest altitudes). Stratificationmay proíe harmful for Ñ. halepensis seeds but is almost always beneficial for theseeds of the latter species.

Some Targets ï[ Future Research

- The quantification of the protection against the heat of fire for the enclosedseeds by surrounding cone tissues.

- Storability and longeíity of seeds - both under controlled environments (ßç thelab or gene banks) and natural conditions (within the cones and ßç the soil).

- Germination ecotypes of Ñ. halepensis ßç regard to the temperature range of seed

germination.- Germination ecotypes of Ñ. brutia ßç regard to stratification requirements, tim-

ing of germination and seed coat properties.- The possible role of íaÞïus chemicals ïç germination at fire-free (e.g. litter)

and post-fire conditions (e.g. nitrates, charate, smoke, etc).- The detrimental role of stratification ßç A1eppo pine seeds; underlying mecha-

nisms and ecological implications.

.References

Calamassi, R. 1982. Effetti della luce e del1a temperatura sulla germinazione dei semi ßç prove-nienze di Pinus halepensis ÌßÉÉ. e Pinus brutia Ten. L' Italia Forestale e Montana 37: 174-187.

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