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(American Journal of Botany. 2008;95:833-842.) doi: 10.3732/ajb.2007354 © 2008 Botanical Society of America, Inc.

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To grow or to seed: ecotypic variation in reproductive allocation and cone production by young female Aleppo pine (Pinus halepensis, Pinaceae)¹

² CIFOR, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Apto. 8111, 28080 Madrid, Spain ³ Banc de Llavors Forestals, Dirección General de Gestión del Medio Natural, Conselleria de Territorio y Vivienda, Avda. Comarques del País Valencià, 144, 46930 Quart de Poblet, Valencia, Spain

Received for publication 31 October 2007. Accepted for publication 28 April 2008.

ABSTRACT

Age and size at the first reproduction and the reproductive allocation of plants are linked to different life history strategies. Aleppo pine only reproduces through seed, and, as such, early female reproduction confers high fitness in its infertile highly fire-prone habitats along the Mediterranean coast because life expectancy is short. We investigated the extent of ecotypic differentiation in female reproductive allocation and examined the relation between early female reproduction and vegetative growth. In a common-garden experiment, the threshold age and size at first female reproduction and female reproductive allocation at age seven differed significantly among Aleppo pine provenances of ecologically distinct origin. Significant correlations among reproductive features of the provenances and the ecological traits of origin were found using different analytical tools. In nonlinear models of cone counts vs. stem volume, medium-sized trees (not the largest trees) produced the highest cone yield, confirming that, at the individual level, early female reproduction is incompatible with fast vegetative growth. The contribution of founder effects and adaptation to contrasting fire regimes may be confounding factors. But considering all traits analyzed, the geographical patterns of resource allocation by Aleppo pine suggest ecotypic specialization for either resource-poor (favoring early reproduction) or resource-rich (favoring vegetative growth) habitats.

Key Words: age at first reproduction • cones • Mediterranean • Pinaceae • Pinus halepensis • reproductive allocation • reproductive effort • threshold size

The trade-offs between resource allocation to reproduction vs. vegetative structures (reproductive allocation) and the relationship between vegetative growth and current reproduction (reproductive effort) are "hot" topics in botanical research, justified by its relevance to plant adaptation (reviewed by Bazzaz and Ackerly, 1992; Obeso, 2002). Following the principles of plant allometry (the relative growth of a part in relation to an entire organism), the differential allocation of resources to reproduction, storage, defense and growth throughout ontogeny is highly specific for species survival strategy (Wilson, 1983; Niklas and Enquist, 2002, 2003). In contrast with the abundant literature on reproductive cost in angiosperms (from herbaceous to woody species), conifers have been relatively neglected (with a few exceptions; see Despland and Houle, 1997; Silvertown and Dodd, 1999). Moreover, the majority of studies on conifers tend to focus on wild populations, while the only data published on intraspecific genetic variation in reproductive traits comes from a few seed-orchard studies (Matziris, 1997, 1998).

Aleppo pine (Pinus halepensis Mill.) is one of the most thoroughly studied Mediterranean conifers, especially with respect to vegetation dynamics under drought and fire disturbances (Daskalakou and Thanos, 1996; Ne’eman and Trabaud, 2000; Ne’eman et al., 2004). As an obligate seeder living in fire-prone habitats, early reproduction is crucial for the species’ fitness, not only in its native habitat, but also as an allochtonous invader in some regions (Barbero et al., 1998; Richardson and Higgins, 1998). Extremely precocious cone bearing by Aleppo pine compared to other pines enables it to accumulate a huge aerial seed bank in serotinous cones at a young age. This seed bank ensures its resilience against stand-replacing cycles occurring at intervals of 30 yr or less (Agee, 1998; Thanos and Daskalakou, 2000; Tapias et al., 2001), but very frequent fires can favor its replacement by seeder shrubs (Pausas and Lloret, 2007). Thinnings in postfire stands have been seen to reduce the time and height for first reproduction (De Las Heras et al., 2007).

Like many other pine species, young Aleppo pines start their reproductive life as females, producing little or no pollen until their crown is structurally well developed. Additionally, in a young stand ovulate strobili contribute much more to reproductive success than do male strobili because efficient pollination is usually accomplished by nearby mature stands (Ne’eman et al., 2004). Hence, we can readily accept that early female reproduction has a higher adaptive value than early male reproduction in Aleppo pine. Considering that high early reproductive effort has a cost for later growth and reproductive success (Obeso, 2002), we suggest that different regional combinations of resource availability and disturbance regime across Aleppo pine’s distribution, have exerted contrasting intraspecific selection pressures on early female reproduction. Both age and size thresholds for female reproduction and the size for maximum reproductive output are relevant when studying the environmental and genetic effects on reproductive precocity in this species because size and not cellular senescence have been reported to account for a great part of ageing phenomena in different tree species (Mencuccini et al., 2005).

High genetic differentiation among populations has been reported in Aleppo pine for neutral (Agúndez et al., 1999; Gómez et al., 2001, 2005) and adaptive traits (Atzmon et al., 2004; Chambel et al., 2007; Voltas et al., in press), suggesting that both nonselective genetic processes and directional selection have contributed significantly to its geographical genetic structure.

We hypothesize that (1) directional selection has caused ecotypic differentiation for female reproductive allocation in Aleppo pine, and (2) at the individual level, assuming that early female reproduction occurs at the expenses of vegetative growth, we would not expect that good growers are the best seeders. To test these hypotheses, we used data collected over nine years in a common-garden experiment containing 53 provenances covering most of Aleppo pine’s range of distribution.

MATERIALS AND METHODS

Plant material
The common-garden experiment included 53 autochthonous provenances from continental Spain, the Balearic Islands, France, Italy, Greece and Tunisia, that we further classified into 15 ecologically distinct regions based on both their environmental similarity and geographical proximity (Gil et al., 1996) (Fig. 1, Appendix 1). The geographical range was from 23°54' E to 4°50' W, and from 36°30' N to 43°24' N, with an altitudinal range from sea level (in some of the Greek, Italian, and Balearic provenances) up to 1238 m a.s.l. (in southern Spain). Open-pollinated seeds from 20 to 30 trees spaced at least 100 m apart were obtained from each population and subsequently bulked into population seedlots. One-year-old seedlings grown in containers were produced following standard nursery practices in 1997.

View larger version (26K): [in this window] [in a new window]   Fig. 1. Location of the 53 studied provenances of Pinus halepensis (black dots), grouped into 15 ecological regions (each represented by a perimeter and acronym). Arrow points to the trial site.

Study site
The trial site was a with a 5% slope located at 39°49'29''N and 00°34'22''W at 640 m a.s.l., within the species natural range in Spain. Soil type was a shallow calcixerollic xerochrept of about 0.5 m depth. Seedlings were planted in a randomized complete block design, with four blocks per provenance and four plants per block (16 trees per provenance) planted at 2.5 x 2.5 m spacing. Mean annual rainfall at the site is 472 mm (22% falling in summer) and mean annual temperature is 13.8°C. The site was chosen as a good representative of Aleppo pine’s ecological niche in Spain, where both climate and soil conditions are moderately limiting. Furthermore, neighboring mature stands acted as complementary pollen sources, ensuring pollination and thus preventing cone abortion (Goubitz et al., 2002). Mortality was negligible (less than 5%) and occurred mostly during the first 3 years of growth.

Variable description
Height was recorded at ages four, seven, and eight years, and basal diameter was recorded at ages four and seven years. Cones were counted yearly from age three (1999) to age nine (2005), covering the transition from mostly vegetative to mostly reproductive (female) individuals. Concomitantly, the occurrence of any multiple female flowering events within the same morphogenetic cycle (Pardos et al., 2003) was recorded as a binary variable (Mf), either the presence or absence of this character in the crown. Individual age (Aff) and height (Hff) at first female flowering were obtained from annual cone counts and periodic height measurements.

Reproductive allocation of each tree, as the static measurement of the ratio of reproductive biomass to total standing biomass (Obeso, 2002), was studied at age seven (summer of 2003), coinciding with a sharp increase in the number of reproductive individuals. We chose stem volume over bark (Vob) as a surrogate for total standing biomass, in preference to height or basal area (Reinhardt et al., 2006). Vob was calculated by the following equation, assuming the stem to be conical:

where Db is basal diameter and H is total tree height.

The biennial cycle of cone development in Aleppo pine (as in most other pines) implies that every year, two strobili cohorts, from two consecutive flowering events, are growing together in the crown. Even when cones usually remain in the crown for more years (serotinous or xeriscent), their dry mass does not increase after their second winter. Considering that these two cohorts compete for the same resources, we defined the variable cone count at age seven (Cc) as the sum of all immature ("green") cones at that age (Fig. 2A, B). We therefore considered reproductive allocation (RA) as the ratio Cc/Vob, in number of cones per cubic decimeter. We also checked for any differences in mean cone dry mass between provenances and for a possible trade-off between cone count and individual cone biomass, by collecting and oven-drying one cone per tree from 352 trees (44% of the total, belonging to all 53 provenances). Because differences between provenances or regions were insignificant and the relationship of cone dry mass to cone counts at the individual level was barely significant and positive (hence, abundant cone production in a tree was associated with bigger, rather than smaller cones), we accepted Cc as a realistic surrogate of female reproductive biomass.

View larger version (139K): [in this window] [in a new window]   Fig. 2. (A) Cone cohorts integrating the variable Cc, in early summer for Pinus halepensis: current year’s female strobili (cn), and previous year’s crop (cn–1). (B) Multiple flowering events from the same calendar year are a common trait in this species; therefore, all green cones, either cn or cn–1 were considered.

where Y is the dependent variable, µ is the general mean, R is the additive effect of ecological region, P is the additive effect of the provenance within ecological region, B is the additive effect of the block, and is the error term. We also considered an alternative model with Vob as a covariate to adjust for the size-dependent variation of RA (Klinkhamer et al., 1992), but this effect was nonsignificant; hence, we decided to stick with the simpler model. Groups of equal means were discriminated using Tukey’s unequal N honestly significant difference (HSD) test (significant at the P < 0.05 level). We used the ratios of sums of squares to compare the proportion of variation explained by each factor.

Nonlinear modeling of reproductive allocation
To complement the analysis of RA as a quotient, we assessed the relationship between the production of female cones and tree size and how this relationship differed geographically by modeling Cc as a function of Vob. Although the literature suggests that there is a consistently positive correlation between vegetative and reproductive biomass irrespective of size (Klinkhamer et al., 1992; Despland and Houle, 1997; Niklas and Enquist, 2003), we checked two alternative relations. (1) Asymptotic. There is an inflection point and a theoretical maximum for reproductive output. Larger trees have more cones, but above a given tree size, there is no further increase in cone production. This relation is expressed by the family of sigmoidal ascending curves. (2) Ascending–descending, with a maximum value. The larger cone crops do not correspond to the larger trees. This relation is expressed by the family of functions with a maximum and an inflection point.

Several biparametric functions of each family were evaluated among those given by (Ratkovsky, 1990). In addition to adjusting the model for pooled individual data, we assumed that observations from trees sharing a common geographical origin were correlated (ecological regions or provenances). This relation was examined in linear and nonlinear mixed models (Lindstrom and Bates, 1990; Davidian and Giltinan, 1995), in which fixed effects were common to the whole meta-population and random effects were specific for each ecological region. Practically, in the first step, both effects (a and b) were assumed to be mixed, divided into a fixed part and a random part, specific to each geographical unit (henceforth referred to as u and v). If convergence was not attained in this way, only one of the effects was considered mixed, while the other was assumed to be fixed. Model comparisons were based on two times the log-likelihood and the sum of squared errors. Smaller estimates for both statistics indicated a more accurate model. Models were fitted by restricted maximum likelihood methods using the MIXED (linear models) or SAS macro NLINMIX (nonlinear models) procedures in the program SAS version no. 8.2 (SAS Institute, Cary, North Carolina, USA). We assessed systematic deviation from the meta-population level model due to each geographical unit using EBLUP (empirical best linear unbiased predictor) for the random effects.

The family of ascending–descending curves gave the best-fit models to explain the observed reproductive allocation patterns. Giving preference to the two times the log-likelihood statistic, we selected the model represented by the equation:

To favor convergence, Vob was transformed to 0.1•Vob. This model implies that the largest cone counts were not produced by the biggest trees, but at Vob_max = –1/b. The maximum cone count, corresponding to this volume, will be referred to as Cc_max. Differences between models were tested using pairwise comparisons in which the complete structure (an independent model for each geographical origin) was compared with the reduced structure (the model is fitted to the pooled data from the two origins) in terms of minus two times the log likelihood.

Relation with geographical and climatic variation
To assess the relation between phenotypic traits and geographical and climate parameters, we used adjusted means for each provenance after removal of block effects and parameters derived from nonlinear models at the scale of ecological regions. Two methodological approaches were applied to characterize the climate of each provenance in the common garden experiment. First, we used the scores of the first two principal components of the climate variables from a principal component analysis. And second, we used the pooled environmental distance between each provenance and the trial site (therefore, calibrating climate data, following Rutter and Fenster [2007]). Gower’s distance (GD) was used for this purpose in the formula:

where p is the number of environmental characteristics, A_i and B_i are the values of those environmental characteristics at the two compared sites and r_i is the total range of the environmental characteristic in the dataset.

RESULTS

Variability among individuals for stem growth and reproductive features
Considering all populations together, mean age at the first flowering event (Aff) was 6.1 yr and ranged from 3 to 9 yr. The threshold height for female flowering (Hff) ranged from 45 to 444 cm with a mean of 163 cm. Reproductive allocation (RA) ranged from 0 to 7.8 cones/dm³ with a mean of 0.5 cones/dm³.

Geographical variation for vegetative and reproductive traits
All the studied variables differed significantly among ecological regions and among provenances within ecological regions (P < 0.005), except for Mf and Cc, which showed marginally nonsignificant provenance effects (Table 1). The influence of ecological region was especially high for Cc, RA, and Hff, while provenances within ecological regions contributed greatly to the variation of stem volume (Vob). Block effects were significant (P < 0.05) for all variables except for Cc and Mf, but contributed little to the variation in Vob and RA. Moreover, the proportion of variation explained by geographical origin (ecological region plus provenance) was highest for RA at 39.2%, contrasting with only 18.9% for stem volume.

View this table: [in this window] [in a new window]   Table 1. ANOVA table (GLM) for the six phenotypic variables analyzed in Pinus halepensis: Vob, stem volume over bark; Aff, age at first flowering; Hff, height at first flowering; Mf, presence of multiple flowering cycles; Cc, count of all immature cones at the crown; RA, reproductive allocation (Cc/Vob). Factors considered as fixed are R, ecological region; P (R), provenance within ecological region; B, block; and , error. Last column is the percentage of the variation explained by each factor, based on sum of squares.

where u and v are random effects dependent on the ecological region. Considering all ecological regions together, Vob_max was 8.7 dm³, corresponding to percentile 67.8. There were large differences among the specific models for each ecological region (Table 3, Fig. 3). While for some provenances (2MO, 8SU, 15TU) the maximum cone yields occurred at low stem volumes, others approximated an asymptotic relationship (14IT, with Cc_max corresponding to volumes close to the maximum values). The values of the quotient Cc_max/Vob_max (Table 3) quantify the steepness of the ascending part of the curve (Fig. 3); hence, it gives a good graphical idea of the maximum reproductive allocation (RA_max). This parameter, RA_max was tightly correlated to RA (r = 0.94, P < 0.001); hence, the ranking for ecological regions was highly conserved between both parameters. Regions 15TU (Tunisia) and 2MO (inland Ebro Depression), together with 8SU (southern Spain) had similar high values for RA_max, and contrasted sharply with the other ecological regions (Table 3). At the other extreme, the Balearic 11PY (Ibiza) and 9MA (Majorca), 1CAT (Catalonia) and Greek (12GR) were tightly grouped with the lowest RA_max. The pairwise model comparisons confirmed the significance of this grouping.

View larger version (15K): [in this window] [in a new window]   Fig. 3. Models of reproductive allocation for each ecological region of Pinus halepensis based on Eq. 5. (A) (B) Vob, volume over bark; Cc count of all immature cones at the crown (see Fig. 2). Codes for the ecological regions are in Appendix 1.

Our study is one of few to demonstrate intraspecific variability for reproductive allocation in a tree species (Aleppo pine). The use of a common-garden experiment (a provenance trial covering most of the species natural area) allowed us to avoid the environmental bias inherent to field studies. Given that our data are based on many provenances tested at a single-site, instead of a reciprocal transplant experiment, we used the calibration to the site conditions as suggested by Rutter and Fenster (2007) to facilitate the comparison of local and increasingly more distant provenances or ecological regions, both geographically and ecologically.

Relation between reproduction and vegetative growth
Nonlinear models of cone production vs. stem volume revealed that, among young, same-aged Aleppo pines, larger cone crops do not correspond to larger trees. Medium-size trees produced the highest cone yields (an average 67.8 percentile for stem volume). This trend is not apparent in the published literature (Klinkhamer et al., 1992; Despland and Houle, 1997; Niklas and Enquist, 2003) and was consistent among ecological regions and provenances (data not shown at provenance level). This supports that precocious and intense female reproduction is incompatible with a high vegetative growth in Aleppo pine. However, there was a significant positive autocorrelation among successive cone counts in our study, suggesting that at the individual level, intense current reproduction does not lead to a significant loss of future reproduction (fecundity cost). This lack of fecundity cost confirms previous observations that periodic intense mast years do not occur in Aleppo pine (Tapias et al., 2001) and contrasts with the behavior of many other tree species, including the closely related Mediterranean stone pine, Pinus pinea (Kelly and Sork, 2002; Mutke et al., 2005b), but see (Knops et al., 2007). Analyses at different within-tree modular levels (branch, shoot, and meristems) should help to unveil the developmental and physiological processes underlying reproductive costs and putative compensation mechanisms.

Ecotypic differentiation for growth and female reproduction in Aleppo pine
Both GLM analysis and specific nonlinear models obtained through EBLUP confirmed our first hypothesis that female reproductive allocation differs significantly among Aleppo pine ecological regions. Because the age and size thresholds for cone bearing (Aff and Hff) were strongly (negatively) correlated with high female reproductive allocation at age seven, the patterns of variation for these three variables were highly coincident. While the minimum age at maturity or age of first reproduction (Aff) has been found to have a high evolutionary significance in woody plants (Keeley and Zedler, 1998; Verdú, 2002), the height for first reproduction seems more related to the environmental variation (expressed by the first principal component of climate variables, Table 5). This higher differentiation for the size threshold for reproduction is coherent with the recent postulation that size is more closely related to the ontogenetic shifts in functional processes than cellular senescence in many tree species (Mencuccini et al., 2005).

Worthy of note, both the first principal component of climate variables and, to a lesser extent, the ecological distance between each provenance and the trial site were significantly correlated with traits linked to precocious and/or abundant reproductive output. In particular, RA was more related to Gower’s distance than to geographical distance, confirming an ecotypic variation for female reproductive allocation.

Plants from the Tunisian ecological region and some Iberian regions (from Ebro basin and southernmost Mediterranean coast) had a marked female reproductive precocity and high reproductive allocation compared with plants from Ibiza, Majorca, Catalonia, and Greece. Across its range of distribution, Aleppo pine has an increasing reproductive allocation and diminishing threshold age and size from east to west and a less marked increasing reproductive allocation toward the south. This geographical pattern mimics an increase in temperature and annual temperature range and a reduction in annual and summer rainfall toward the western and southern edges of the distributional range. An adaptive shift from vegetative to reproductive meristems in response to stressful or resource-poor environments for southern and western provenances (extreme temperatures, lower rainfall, and shallow soils) can be invoked to explain this trend, similarly to that reported for Arabidopsis (Bonser and Aarssen, 2001, but see Sakai et al., 2006).

The high ecotypic differentiation for reproductive features among provenances contrasts with a low differentiation for vegetative growth, represented by stem volume. Only the Greek provenances stood out from the rest, surprisingly similar to each other. This outlier behavior of fast-growing Greek provenances has been corroborated in different common garden experiments (Matziris, 2000; Chambel et al., 2007). The lack of significant ecotypic variation for growth in Aleppo pine parallels findings in other Mediterranean pines, such as the Canary Island pine (Pinus canariensis) (López et al., 2007) and the Mediterranean stone pine (Pinus pinea) (Mutke et al., 2007, 2008) and suggests a low fitness value of vegetative growth per se in these pines living in disturbed and seasonally dry environments. This intriguing common pattern should be studied considering the trade-offs between resilience (either through resprouting or sexual reproduction) and growth (Pausas et al., 2004; Schwilk and Ackerly, 2005).

Alternative interpretations and perspectives
There are two alternative causal factors for the geographical variation in early reproduction by female Aleppo pines. One is an effect of fire regime, based on the known adaptive value of early and intense reproduction against stand-replacing fires in obligate seeders (Schwilk and Ackerly, 2001). Lightning fires are rare in the eastern Mediterranean, but in the western part of Aleppo pine’s distribution they are quite frequent (Vázquez and Moreno, 1998; Ne’eman et al., 2004). The lower levels of serotiny in natural Aleppo pine provenances from Greece and Israel compared to those from the Iberian Peninsula have been postulated to correspond to a higher adaptation to fire in the western part of the species range (Tapias et al., 2001). Hence, the westward decrease in the threshold size for reproduction shown by our experiment could also reflect divergent evolution related to different natural fire regimes, as proposed for other taxa (Zammit, 1987; Keeley and Zedler, 1998; Climent et al., 2004; Tapias et al., 2004).

Our second alternative explanation for geographical variation in female reproduction is population founder effects. Considering that high reproductive allocation is typical of colonizing or expanding populations (Obeso, 2002), the divergence of reproductive features in Aleppo pine can be interpreted with respect to the species postglacial dynamics in the Mediterranean basin. The relatively recent (8000–10000 yr) spread of Pinus halepensis following a general migration from northeast to southwest has been well established using various biochemical and DNA markers (Barbero et al., 1998; Agúndez et al., 1999; Gómez et al., 2005). The coincidence of colonization routes and climatic gradients hampers separating between founder effect and local ecotypic adaptation. The island populations along the Mediterranean can perhaps provide a good sampling system to further confirm the extent of founder effects in the geographical variation of Aleppo pine.

We are aware that this work opens many research fronts. Further research is needed to understand the evolutionary interplay between contrasting fire regimes and early reproductive allocation in this fire-resilient species, and male reproduction should also be considered at higher developmental stages. This need is urgent, considering the increased frequency of catastrophic forest fires during the last few decades across the range of Aleppo pine and the predictions of more severe droughts and higher temperatures for the Mediterranean basin. Outside the species’ natural range, this knowledge will help to establish better controls to minimize its invasive potential.

Appendix 1. Region (Reg.) and main climate characteristics of the studied provenances (Prov.) of Pinus halepensis. Alt: Altitude; T: mean annual temperature; TAR: annual temperature range; P: annual rainfall; Ps: summer rainfall (June, July and August).

FOOTNOTES

¹ Thanks to D. Agúndez for previous work on the Pinus halepensis provenance trial and to F. Del Caño and S. Herrera for fieldwork. Special thanks to R. Tapias, S. Mutke, P. Aravanopoulos, and B. Lovatom for critical readings and helpful comments. Funding was provided by the Spanish Directorate for Biodiversity (DGB, Ministry of Environment, CC03-048). J.C. was funded by the Spanish Ministry of Education and Science (Ramón y Cajal program). Matt Robson edited the English.

⁴ Author for correspondence (e-mail: climent{at}inia.es)

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