Positive coupling between growth and reproduction in young post-fire Aleppo pines depends on climate and site conditions
Raquel Alfaro-Sánchez A E , J. Julio Camarero B , Francisco R. López-Serrano A , Raúl Sánchez-Salguero C D , Daniel Moya A and Jorge De Las Heras A
+ Author Affiliations
- Author Affiliations
A Department of Plant Production and Agricultural Technology, ETSIA, Universidad de Castilla-La Mancha, Campus Universitario s/n, 02071 Albacete, Spain.
B Instituto Pirenaico de Ecología (IPE-CSIC), CSIC, Avda. Montaña, 1005, 50192 Zaragoza, Spain.
C Departamento de Ingeniería Forestal, Laboratorio de Dendrocronología, Universidad de Córdoba, Campus de Rabanales, N-IV, km 396, 14071 Córdoba, Spain.
D Swiss Federal Research Institute WSL, Zurcherstrasse 111, 8903 Birmensdorf, Switzerland.
E Corresponding author. Email: r.alfarosanchez@gmail.com
International Journal of Wildland Fire 24(4) 507-517 https://doi.org/10.1071/WF14045
Submitted: 25 March 2014 Accepted: 10 November 2014 Published: 1 June 2015
Abstract
In fire- and drought-prone Mediterranean forests tree growth and regeneration depend on the moisture regime between fires. Therefore, post-fire tree regeneration will depend on moisture conditions and how they are altered by fire recurrence and climate warming. Aleppo pine forests are the most abundant Circum-Mediterranean ecosystems subjected to frequent wildfires and summer droughts. Because both stressors constrain their reproduction and growth patterns across diverse ecological conditions, these forests represent a suitable system to test how moisture availability drives post-fire regeneration. Aleppo pine is an obligate seeder species that reproduces at an early age after fire. Such precocious behaviour poses the question as to whether post-fire regeneration depends on moisture conditions and the coupling between female cone production and growth. Here, we evaluate if female cone production and radial growth are linked at the tree level in post-fire Aleppo pines by comparing a dry v. a very dry site and considering stands with three different tree densities in south-eastern Spain. We found that trees with higher basal areas produced more female cones and this positive association intensified as the water balance improved. Aleppo pines from the very dry site were more precocious in reproductive terms than pines of the same age from the dry site, but long-term cone production was lower at the very dry site. Lower tree density enhances the resilience of xeric post-fire Aleppo pine forests, in growth and reproduction terms, but this effect can be reversed by droughts. Overall, a more positive water balance improves post-fire regeneration by enhancing growth and cone production. Thus, silvicultural treatments such as thinning should be applied by taking into account the post-fire water balance to maximise growth and cone production in Aleppo pine stands. Our findings illustrate how climate warming could hamper post-fire tree regeneration by aggravating drought stress.
Additional keywords: drought, Pinus halepensis, post-fire reproduction, radial growth, serotiny.
References
Bates DM, Maechler M, Bolker B (2013) Package lme4: linear mixed-effects models using S4 classes. Available at http://CRAN.R-project.org/package=lme4 [Verified 22 December 2014]Borghetti M, Cinnirella S, Magnani F, Saracino A (1998) Impact of long-term drought on xylem embolism and growth in Pinus halepensis Mill. Trees – Structure and Function 12, 187–195.
Burnham KP, Anderson DR (2002) ‘Model selection and multimodel inference: a practical information-theoretic approach.’ (Springer: New York)
Calama R, Mutke S, Tomé J, Gordo J, Montero G, Tomé M (2011) Modelling spatial and temporal variability in a zero-inflated variable: the case of Stone pine (Pinus pinea L.) cone production. Ecological Modelling 222, 606–618.
| Modelling spatial and temporal variability in a zero-inflated variable: the case of Stone pine (Pinus pinea L.) cone production.Crossref | GoogleScholarGoogle Scholar |
Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytologist 185, 471–480.
| Plastic bimodal xylogenesis in conifers from continental Mediterranean climates.Crossref | GoogleScholarGoogle Scholar | 19895415PubMed |
Climent J, Prada MA, Calama R, Chambel MR, De Ron DS, Alía R (2008) To grow or to seed: ecotypic variation in reproductive allocation and cone production by young female Aleppo pine (Pinus halepensis, Pinaceae). American Journal of Botany 95, 833–842.
| To grow or to seed: ecotypic variation in reproductive allocation and cone production by young female Aleppo pine (Pinus halepensis, Pinaceae).Crossref | GoogleScholarGoogle Scholar | 21632409PubMed |
Corona P, Leone V, Saracino A (1998) Plot size and shape for the early assessment of post-fire regeneration in Aleppo pine stands. New Forests 16, 213–220.
| Plot size and shape for the early assessment of post-fire regeneration in Aleppo pine stands.Crossref | GoogleScholarGoogle Scholar |
Daskalakou EN, Thanos CA (1996) Aleppo pine (Pinus halepensis) postfire regeneration: the role of canopy and soil seed banks. International Journal of Wildland Fire 6, 59–66.
| Aleppo pine (Pinus halepensis) postfire regeneration: the role of canopy and soil seed banks.Crossref | GoogleScholarGoogle Scholar |
De Las Heras J, González-Ochoa A, López-Serrano F, Simarro ME (2004) Effects of silviculture treatments on vegetation after fire in Pinus halepensis Mill. woodlands (SE Spain). Annals of Forest Science 61, 661–667.
| Effects of silviculture treatments on vegetation after fire in Pinus halepensis Mill. woodlands (SE Spain).Crossref | GoogleScholarGoogle Scholar |
De Las Heras J, Moya D, Lopez-Serrano FR, Condes S (2007) Reproduction of postfire Pinus halepensis Mill. stands six years after silvicultural treatments. Annals of Forest Science 64, 59–66.
| Reproduction of postfire Pinus halepensis Mill. stands six years after silvicultural treatments.Crossref | GoogleScholarGoogle Scholar |
de Luis M, Gricǎr J, Cǔfar K, Raventós J (2007) Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain. IAWA Journal 28, 389–404.
| Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain.Crossref | GoogleScholarGoogle Scholar |
Espelta JM, Verkaik I, Eugenio M, Lloret F (2008) Recurrent wildfires constrain long-term reproduction ability in Pinus halepensis Mill. International Journal of Wildland Fire 17, 579–585.
| Recurrent wildfires constrain long-term reproduction ability in Pinus halepensis Mill.Crossref | GoogleScholarGoogle Scholar |
Espelta JM, Arnan X, Rodrigo A (2011) Non-fire induced seed release in a weak serotinous pine: climatic factors, maintenance costs or both? Oikos 120, 1752–1760.
| Non-fire induced seed release in a weak serotinous pine: climatic factors, maintenance costs or both?Crossref | GoogleScholarGoogle Scholar |
Esteban LG, Martin JA, de Palacios P, García-Fernández F, López R (2010) Adaptive anatomy of Pinus halepensis trees from different Mediterranean environments in Spain. Trees 24, 19–30.
| Adaptive anatomy of Pinus halepensis trees from different Mediterranean environments in Spain.Crossref | GoogleScholarGoogle Scholar |
Eugenio M, Verkaik I, Lloret F, Espelta JM (2006) Recruitment and growth decline in Pinus halepensis populations after recurrent wildfires in Catalonia (NE Iberian Peninsula). Forest Ecology and Management 231, 47–54.
| Recruitment and growth decline in Pinus halepensis populations after recurrent wildfires in Catalonia (NE Iberian Peninsula).Crossref | GoogleScholarGoogle Scholar |
Girard F, Vennetier M, Guibal F, Corona C, Ouarmim S, Herrero A (2012) Pinus halepensis Mill. crown development and fruiting declined with repeated drought in Mediterranean France. European Journal of Forest Research 131, 919–931.
| Pinus halepensis Mill. crown development and fruiting declined with repeated drought in Mediterranean France.Crossref | GoogleScholarGoogle Scholar |
González-Ochoa AI, López-Serrano FR, De las Heras J (2004) Does post-fire forest management increase tree growth and cone production in Pinus halepensis? Forest Ecology and Management 188, 235–247.
| Does post-fire forest management increase tree growth and cone production in Pinus halepensis?Crossref | GoogleScholarGoogle Scholar |
Goubitz S, Nathan R, Roitemberg R, Shmida A, Ne’eman G (2004) Canopy seed bank structure in relation to: fire, tree size and density. Plant Ecology 173, 191–201.
| Canopy seed bank structure in relation to: fire, tree size and density.Crossref | GoogleScholarGoogle Scholar |
Hargreaves GH, Samani ZA (1985) Reference crop evapotranspiration from temperature. Applied Engineering in Agriculture 1, 96–99.
| Reference crop evapotranspiration from temperature.Crossref | GoogleScholarGoogle Scholar |
Haymes KL, Fox GA (2012) Variation among individuals in cone production in Pinus palustris (Pinaceae). American Journal of Botany 99, 640–645.
| Variation among individuals in cone production in Pinus palustris (Pinaceae).Crossref | GoogleScholarGoogle Scholar | 22434774PubMed |
Hernández-Serrano A, Verdú M, González-Martínez SC, Pausas J (2013) Fire structures pine serotiny at different scales. American Journal of Botany 100, 2349–2356.
| Fire structures pine serotiny at different scales.Crossref | GoogleScholarGoogle Scholar | 24222682PubMed |
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bulletin 43, 69–78.
Keeley JE, Zedler PH (1998) Evolution of life histories in Pinus. In ‘Ecology and biogeography of Pinus’. (Ed. DM Richardson) pp. 219–250. (Cambridge University Press: Cambridge)
Klein T, Hoch G, Yakir D, Körner Ch (2014) Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest. Tree Physiology
| Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest.Crossref | GoogleScholarGoogle Scholar | 25187568PubMed |
Knops JMH, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proceedings of the National Academy of Sciences of the United States of America 104, 16 982–16 985.
| Negative correlation does not imply a tradeoff between growth and reproduction in California oaks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1KgtLbN&md5=0232dc962ff722a0a519a15ac986e69eCAS |
Linares JC, Camarero JJ, Carreira JA (2010) Competition modulates the adaptation capacity of forests to climatic stress: insights from recent growth decline and death in relict stands of the Mediterranean fir Abies pinsapo. Journal of Ecology 185, 471–480.
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997.
| More intense, more frequent, and longer lasting heat waves in the 21st century.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVGmtrc%3D&md5=c54f20e3a0c690a789819625a489590eCAS | 15310900PubMed |
Misson L, Vincke C, Devillez F (2003) Frequency responses of radial growth series after different thinning intensities in Norway spruce (Picea abies (L.) Karst.) stands. Forest Ecology and Management 177, 51–63.
| Frequency responses of radial growth series after different thinning intensities in Norway spruce (Picea abies (L.) Karst.) stands.Crossref | GoogleScholarGoogle Scholar |
Moya D, De las Heras J, López-Serrano FR, Leone V (2008a) Optimal intensity and age of management in young Aleppo pine stands for post-fire resilience. Forest Ecology and Management 255, 3270–3280.
| Optimal intensity and age of management in young Aleppo pine stands for post-fire resilience.Crossref | GoogleScholarGoogle Scholar |
Moya D, Espelta J, López-Serrano FR, Eugenio M, De las Heras J (2008b) Natural post-fire dynamics and serotiny in 10-year-old Pinus halepensis Mill. stands along a geographic gradient. International Journal of Wildland Fire 17, 287–292.
| Natural post-fire dynamics and serotiny in 10-year-old Pinus halepensis Mill. stands along a geographic gradient.Crossref | GoogleScholarGoogle Scholar |
Mudelsee M (2003) Estimating Pearson’s correlation coefficient with bootstrap confidence interval from serial dependent time series. Mathematical Geology 35, 651–665.
| Estimating Pearson’s correlation coefficient with bootstrap confidence interval from serial dependent time series.Crossref | GoogleScholarGoogle Scholar |
Nathan R, Safriel UN, Noy-Meir I, Schiller G (1999) Seed release without fire in Pinus halepensis, a Mediterranean serotinuous wind-dispersed tree. Journal of Ecology 87, 659–669.
| Seed release without fire in Pinus halepensis, a Mediterranean serotinuous wind-dispersed tree.Crossref | GoogleScholarGoogle Scholar |
Nathan R, Safriel UN, Noy-Meir I, Schiller G (2000) Spatio temporal variation in seed dispersal and recruitment near and far from Pinus halepensis trees. Ecology 81, 2156–2169.
| Spatio temporal variation in seed dispersal and recruitment near and far from Pinus halepensis trees.Crossref | GoogleScholarGoogle Scholar |
Naveh Z (1974) Effects of fire in the Mediterranean region. In ‘Fire and ecosystems’. (Eds TT Kozlowski, CE Ahlgren) pp. 401–434. (Academic Press: New York)
Ne’eman G, Goubitz S, Nathan R (2004) Reproductive traits of Pinus halepensis in the light of fire – a critical review. Plant Ecology 171, 69–79.
| Reproductive traits of Pinus halepensis in the light of fire – a critical review.Crossref | GoogleScholarGoogle Scholar |
Ne’eman G, Goubitz S, Werger MJA, Shmida A (2011) Relationships between tree size, crown shape, gender segregation and sex allocation in Pinus halepensis, a Mediterranean pine tree. Annals of Botany 108, 197–206.
| Relationships between tree size, crown shape, gender segregation and sex allocation in Pinus halepensis, a Mediterranean pine tree.Crossref | GoogleScholarGoogle Scholar | 21586528PubMed |
Olivar J, Bogino S, Spiecker H, Bravo F (2012) Climate impact on growth dynamic and intra-annual density fluctuations in Aleppo pine (Pinus halepensis) trees of different crown classes. Dendrochronologia 30, 35–47.
| Climate impact on growth dynamic and intra-annual density fluctuations in Aleppo pine (Pinus halepensis) trees of different crown classes.Crossref | GoogleScholarGoogle Scholar |
Ortiz O, Ojeda G, Espelta JM, Alcañiz JM (2012) Improving substrate fertility to enhance growth and reproductive ability of a Pinus halepensis Mill. afforestation in a restored limestone quarry. New Forests 43, 365–381.
| Improving substrate fertility to enhance growth and reproductive ability of a Pinus halepensis Mill. afforestation in a restored limestone quarry.Crossref | GoogleScholarGoogle Scholar |
Panetsos KP (1981) Monograph of Pinus halepensis Mill. and P. brutia Ten. Annales Forestales 9, 39–77.
Pasho E, Camarero JJ, Vicente-Serrano SM (2012) Climatic impacts and drought control of radial growth and seasonal wood formation in Pinus halepensis. Trees – Structure and Function 26, 1875–1886.
| Climatic impacts and drought control of radial growth and seasonal wood formation in Pinus halepensis.Crossref | GoogleScholarGoogle Scholar |
Pausas JG (2004) Changes in fire and climate in the eastern Iberian peninsula (Mediterranean Basin). Climatic Change 63, 337–350.
| Changes in fire and climate in the eastern Iberian peninsula (Mediterranean Basin).Crossref | GoogleScholarGoogle Scholar |
Piñol J, Terradas J, Lloret F (1998) Climate warming, wildfire hazard, and wildfire occurrence in coastal eastern Spain. Climatic Change 38, 345–357.
| Climate warming, wildfire hazard, and wildfire occurrence in coastal eastern Spain.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2014) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing:Vienna) Available at http://www.R-project.org [verified 9 December 2014]
Richardson DM (2000) Mediterranean pines as invaders in the Southern Hemisphere. In ‘Ecology, biogeography, and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean basin’. (Eds G Ne’eman, L Trabaud) pp. 131–142. (Backhuys Publishers: Leiden)
Rivas-Martínez S, Sánchez-Mata D, Costa M (1999) North American boreal and western temperate forest vegetation. Itinera Geobotanica 12, 5–316.
Ruano I, Rodríguez-García E, Bravo F (2013) Effects of pre-commercial thinning on growth and reproduction in post-fire regeneration of Pinus halepensis Mill. Annals of Forest Science 70, 357–366.
| Effects of pre-commercial thinning on growth and reproduction in post-fire regeneration of Pinus halepensis Mill.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Gallardo JR, Castaño S, Calera A (2004) Application of remote sensing and GIS to locate priority intervention areas after wildland fires in Mediterranean systems: a case study from south-eastern Spain. International Journal of Wildland Fire 13, 241–252.
| Application of remote sensing and GIS to locate priority intervention areas after wildland fires in Mediterranean systems: a case study from south-eastern Spain.Crossref | GoogleScholarGoogle Scholar |
Santos-del-Blanco L, Bonser SP, Valladares F, Chambel MR, Climent J (2013) Plasticity in reproduction and growth among 52 range-wide populations of a Mediterranean conifer: adaptive responses to environmental stress. Journal of Evolutionary Biology 26, 1912–1924.
| Plasticity in reproduction and growth among 52 range-wide populations of a Mediterranean conifer: adaptive responses to environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sfps1ajsQ%3D%3D&md5=4b03dd2a98fac1cf0cb96e61765e3323CAS | 23944274PubMed |
Tapias R, Gil L, Fuentes-Utrilla P, Pardos JA (2001) Canopy seed banks in Mediterranean pines of south-eastern Spain: a comparison between Pinus halepensis Mill., P. pinaster Ait., P. nigra Arn. and P. pinea L. Journal of Ecology 89, 629–638.
| Canopy seed banks in Mediterranean pines of south-eastern Spain: a comparison between Pinus halepensis Mill., P. pinaster Ait., P. nigra Arn. and P. pinea L.Crossref | GoogleScholarGoogle Scholar |
Thanos AT, Daskalakou EN (2000) Reproduction in Pinus halepensis and Pinus brutia. In ‘Ecology, biogeography and management of Pinus halepensis and Pinus brutia forest ecosystems in the Mediterranean Basin’. (Eds G Ne’eman, L Trabaud) pp. 79–90. (Backhuys Publishers: Leiden)
Thomas SC (2011) Age-related changes in tree growth and functional biology: the role of reproduction. In ‘Size- and age-related changes in tree structure and function’. (Eds FC Meinzer, B Lachenbruch, TE Dawson) pp. 33–64. (Springer: Heidelberg)
Thornley JHM, Johnson IR (1990) ‘Plant and crop modelling.’ (Blackburn: Caldwell)
Trabaud L (1987) Fire and survival traits in plants. In ‘The role of fire in ecological systems’. (Ed. L Trabaud) pp. 65–90. (SPB Academic Publishers: The Hague)
Verkaik I, Espelta JM (2006) Post-fire regeneration thinning, cone production, serotiny and regeneration age in Pinus halepensis. Forest Ecology and Management 231, 155–163.
| Post-fire regeneration thinning, cone production, serotiny and regeneration age in Pinus halepensis.Crossref | GoogleScholarGoogle Scholar |
Wright SJ, Jaramillo MA, Pavon J, Condit R, Hubbell SP, Foster RB (2005) Reproductive size thresholds in tropical trees: variation among individuals, species and forests. Journal of Tropical Ecology 21, 307–315.
| Reproductive size thresholds in tropical trees: variation among individuals, species and forests.Crossref | GoogleScholarGoogle Scholar |
