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Fire Structures Pine Serotiny at Different Scales

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Fire Structures Pine Serotiny at Different Scales American Journal of Botany 100(12): 2349–2356. 2013. F IRE STRUCTURES PINE SEROTINY AT DIFFERENT SCALES 1 A NA H ERNÁNDEZ-SERRANO 2 , M IGUEL V ERDÚ 2 , S ANTIAGO C. GONZÁLEZ-MARTÍNEZ 3 , AND J ULI G. PAUSAS 2,4 2 CIDE-CSIC, Ctra. Nàquera Km. 4.5 (IVIA campus) 46113 Montcada, Valencia, Spain; and 3 CIFOR-INIA, Ctra. A Coruña Km 7.5 28040 Madrid, Spain • Premise of the study: Serotiny (delayed seed release with the consequent accumulation of a canopy seedbank) confers fi tness benefi ts in environments with crown-fi re regimes. Thus, we predicted that serotiny level should be higher in populations recur- rently subjected to crown-fi res than in populations where crown-fi res are rare. In addition, under a high frequency of fi res, space and resources are recurrently available, permitting recruitment around each mother to follow the seed rain shadow. Thus, we also predicted spatial aggregation of serotiny within populations. • Methods: We compared serotiny, considering both the proportion and the age of serotinous cones, in populations living in contrasting fi re regimes for two iconic Mediterranean pine species (Pinus halepensis , P. pinaster ). We framed our results by quantitatively comparing the strength of the fi re–serotiny relationship with previous studies worldwide. • Key results: For the two species, populations living under high crown-fi re recurrence regimes had a higher serotiny level than those populations where the recurrence of crown-fi res was low. For P. halepensis (the species with higher serotiny), popula- tions in high fi re recurrence regimes had higher fi ne-scale spatial aggregation of serotiny than those inhabiting low fi re recur- rence systems. The strength of the observed fi re–serotiny relationship in P. halepensis is among the highest in published literature. • Conclusions: Fire regime shapes serotiny level among populations, and in populations with high serotiny, recurrent fi res main- tain a signifi cant spatial structure for this trait. Consequently, fi re has long-term evolutionary implications at different scales, emphasizing its prominent role in shaping the ecology of pines. Key words: fi re ecology; Pinaceae; Pinus halepensis ; Pinus pinaster ; seed bank; serotiny; spatial structure. Fire is a major ecological factor in many ecosystems, and 2012 ). Consequently, the dynamics of serotinous populations therefore, plants have developed traits to cope with recurrent follow postfi re pulses of recruitment, in contrast to nonseroti- fi res ( Pausas et al., 2004 ; Pausas and Keeley, 2009 ). There is nous populations that may produce recruits in any year. Se- an increasing bulk of information suggesting that different fi re rotiny can be disaggregated in two components, the proportion regimes may act as an evolutionary force shaping plant traits of serotinous cones and the time these cones remain closed on ( Keeley et al., 2011 ; Pausas and Schwilk, 2012 ; He et al., the plant ( Midgley, 2000 ). A given level of serotiny can be 2012 ). One of the most apparent traits related to fi re is se- achieved by accumulating many weak (short-lived) serotinous rotiny, that is, the delayed seed release for more than a year, cones or few strong (long-lived) serotinous cones across years. requiring an environmental stimulus (a heat shock) for disper- However, the two components have rarely been simultane- sal. The consequence of this delay is the retention of seeds in ously considered. “cones” (conifer cones or woody fruits) in the canopy for Serotiny is variable not only among closely related species more than one reproductive cycle (canopy seed bank; Lamont ( Keeley and Zedler, 1998 ; Lamont et al., 1991 ; He et al., 2012 ) et al., 1991 ). By delaying dispersal until a fi re occurs, seroti- but also within and among populations of a single species ( Muir nous species recruit in postfi re conditions with high resource and Lotan, 1985 ; Schoennagel et al., 2003 ; Tapias et al., 2004 ). availability, low competition, and low predation (predator There is evidence that serotiny increases with the frequency of saturation), and thus, serotiny confers fi tness advantages in crown fi res ( Gauthier et al., 1996 ; Radeloff et al., 2004 ), and ecosystems under crown-fi re regimes ( Lamont et al., 1991 ; even a single fi re may increase the population serotiny level Keeley and Zedler, 1998 ; Lamont and Enright, 2000 ; He et al., given enough variability of the trait in the population ( Muir and Lotan, 1985 ; Goubitz et al., 2004 ). However, variability in the 1 Manuscript received 19 May 2013; revision accepted 11 September strength of the fi re–serotiny relationship remains unexplored. 2013. In addition, there is a lack of information on the within-popula- The authors thank Katharina Budde, Mario Zabal-Aguirre, Diana Turrión tion variability in serotiny. Such variability may have profound and Jordi Chofre for fi eld assistance. This study was fi nanced by the following implications for dynamic processes. Crown fi res could act as a projects supported by the Spanish government: VAMPIRO (CGL2008- selective force favoring the establishment of the offspring of 05289-C02-01/02), LinkTree (ERAnet-BiodivERsA: EUI2008-03713 and serotinous individuals ( Givnish, 1981 ). As far as we know, there EUI2008-03721), VIRRA (CGL2009-12048/BOS), SOBACO (CGL2011- are no explicit measures of fi tness advantages of serotinous in- 29585-C02), and TREVOL (CGL2012-39938-C02-01). CIDE is a joint dividuals. However, the evidence of genetic control of serotiny institute of the Spanish Research Council (CSIC), the Generalitat Valenciana , and the University of Valencia. The authors have no confl ict of ( Perry and Lotan, 1979 ; Tapias et al., 2004 ), together with the interest to declare. higher serotiny in recurrently burnt ecosystems points toward 4 Author for correspondence (e-mail: [email protected]) fi re as a selective force. Within-population variability in serotiny can be spatially doi:10.3732/ajb.1300182 structured at different scales ( Tinker et al., 1994 ). In fact, American Journal of Botany 100(12): 2349–2356, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America 2349 2350 AMERICAN JOURNAL OF BOTANY [Vol. 100 contrasting fi re regimes can produce different spatial pat- under these conditions, most regeneration events are driven by fi re (HiFi terns of serotiny through processes related to natural regen- populations). The remaining six populations were located inland at higher eration dynamics. Under a high frequency of fi res, space and altitudes and subject to subhumid climate, where crown-fi res are rare and most regeneration events are independent of fi re (LoFi populations) ( Verdú resources are recurrently available for recruitment (after and Pausas, 2007 ). In the study area, fi re is strongly linked to climatic condi- each fi re), potentially permitting the recruitment to be spa- tions, specifically to drought ( Pausas, 2004 ). Furthermore, recent fi re history tially aggregated around each mother (refl ecting the seed information ( Pausas, 2004 ; Pausas and Fernández-Muñoz, 2012 ) shows that rain shadow). In contrast, in the absence of fi re, recruitment more than 50% of the study area at <800 m a.s.l. (HiFi conditions) burned at depends on the availability of safe sites and is not necessar- least once during the 1978–2001 period, while for >800 m a.s.l. (LoFi condi- ily spatially aggregated, but driven by gap dynamics related tions), the proportion was about 15% ( Abdel Malak and Pausas, 2006 ). That is, despite the lack of long-term fi re statistics for the specifi c study sites, there to disturbances other than fi re. Consequently, and assuming is strong evidence that the fi re interval is much shorter in HiFi areas than in that the level of serotiny is heritable ( Perry and Lotan, 1979 ; LoFi. In the study area, fertility is strongly related to nature of the bedrock Budde et al., 2013 ) and that there is marked intrapopulation type (siliceous bedrocks are typically nutrient-poorer than calcareous bed- variation in levels of serotiny, we would expect a more aggre- rocks; Ojeda et al., 2010 ); all P. pinaster populations were on siliceous soils, gated spatial pattern of matched serotiny levels in recurrently while P. halepensis included sites in siliceous and in calcareous soils in both burnt ecosystems than in systems that rarely burn. In other HiFi and LoFi conditions (Appendix S1). words, if there are variations in serotiny among individuals within the population, and if the majority of seed dispersal is Sampling — We selected and geo-referenced 40 to 67 individuals in each population including a wide range of distances between trees (Appendix S1) within short distances (postfi re conditions), a spatial aggrega- but avoiding subcanopy trees and trees with diameters less than 10 cm. There tion is likely. In addition, postrecruitment mortality erases ini- were no differences in mean tree diameter between HiFi and LoFi populations tial spatial aggregated patterns driven by dispersal ( Steinitz et al., for any of the species ( P. halepensis : p = 0.4; P. pinaster : p = 0.1; linear mixed 2011 ); thus, the lower the recurrence of fi re the less the aggre- models considering population as random factor; Appendix S1). Serotiny was gation pattern of serotiny is expected. estimated considering both the proportion of serotinous cones and the cone Our hypothesis was that contrasted fi re regimes should pro- age. In each individual, we fi rst searched for the oldest serotinous cone. The age of each cone was estimated by counting the number of internodes from duce different spatial patterns of serotiny for both within and the tip to the location of the cone. Then we counted and dated serotinous between populations. These differences are predicted to in- (closed) and nonserotinous (open or partially open) cones in two opposite crease with the serotiny level of the species. Specifi cally, we branches belonging to the upper third of the canopy and in two opposite expected higher serotiny levels and more spatially aggregated branches contained in the second third of the canopy.
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