Abstract
Key message
The Mexican beech undergoes masting events, on average, every 5.5 years. These events depend directly on precipitation.
Abstract
Climate change has considerably impacted the protective functions of tropical montane cloud forests, possibly influencing the synchronicity of phenological processes and the distribution and physiology of plants. In particular, climatic fluctuations cause changes in the distribution of tree species. Mexican beech (Fagus grandifolia subsp. mexicana) is considered an endangered species, due to its restricted distribution and its being a Miocene relict, limited to tropical montane cloud forests in the mountains of the Sierra Madre Oriental in eastern Mexico. We analyzed the influence of temperature and precipitation in prompting changes to tree-ring width, as well as vessel frequency and diameter, of Mexican beech in eastern Mexico. We used growth rings and xylem vessels traits to infer the historical masting events of Mexican beech over the last 128 years. We obtained independent chronologies for Mexican beech in each of the studied sites, dating back 152–178 years. Precipitation was strongly associated with differences in tree-ring width between masting and non-masting years. Our study highlights the use of dendroecological research to detect climate-induced modifications in the vessel frequency and diameter of tree species inhabiting tropical montane cloud forests. This association also explained differences in vessel frequency and diameter recorded before, during, and after masting events. Our results revealed that Mexican beech undergoes masting events every 5.5 years on average, and that these events directly depend on minimum annual precipitation. In conclusion, our results advance our understanding on the plasticity of growth rings and vessels traits (frequency and diameter) in response to fluctuation in precipitation.
Similar content being viewed by others
References
Abrantes J, Campelo F, García-González I, Nabais C (2013) Environmental control of vessel traits in Quercus ilex under Mediterranean climate: relating xylem anatomy to function. Trees 27:655–662
Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204
Amoroso MM, Daniels LD, Baker PJ, Camarero JJ (2017) Dendroecology: tree-ring analyses applied to ecological studies. Springer, Switzerland
Anderegg WRL, Meinzer FC (2015) Wood anatomy and plant hydraulics in a changing climate. In: Hake U (ed) Functional and ecological xylem anatomy. Springer, Switzerland, pp 235–253
Arlot S, Celisse A (2010) A survey of cross-validation procedures for model selection. Stat Surv 4:40–79
Ascoli D, Vacchiano G, Turco M, Conedera M, Drobyshev I, Maringer J, Motta R, Hacket-Pain A (2017) Inter-annual and decadal changes in teleconnections drive continental-scale synchronization of tree reproduction. Nat Commun 8(2205):1–9
Bayramzadeh V, Funada R, Kubo T (2008) Relationships between vessel element anatomy and physiological as well as morphological traits of leaves in Fagus crenata seedlings originating from different provenances. Trees 22:217–224
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Use R! series. Springer, New York
Box GEP, Jenkins GM (1976) Time series analysis: forecasting and control. Holden-Day, San Francisco
Bradshaw RHW, Kito K, Gieseckre T (2010) Factors influencing the Holocene history of Fagus. For Ecol Manag 259:2204–2212
Bryukhanova M, Fonti P (2013) Xylem plasticity allows rapid hydraulic adjustment to annual climatic variability. Trees 27:485–496
Burns KC (2012) Masting in a temperate tree: evidence for environmental prediction. Austral Ecol 37:175–182
Cardoza-Martínez GF, Cerano-Paredes J, Villanueva-Díaz J, Cervantes-Martínez R, Guerra de la Cruz V, Estrada-Ávalos J (2013) Annual precipitation reconstruction of the Eastern region of Tlaxcala state. Rev Mex Cie Forest 5:110–127
Chan BC, Cain JC (1967) The effect of seed formation on subsequent flowering in apple. J Am Soc Hortic Sci 91:63–68
Climate-data.org (2016) Historical average temperature. http://climate-data.org/. Accessed 10 Oct 2016
Cook ER, Holmes RL (1995) Guide for computer program ARSTAN. In: Grissino-Mayer HD, Holmes RL, Fritts HC (eds) The International tree-ring data bank program library version 2.0 User’s Manual, Laboratory of Tree-Ring Research. University of Arizona, Arizona, pp 75–87
Cook ER, Holmes RL (1999) Program ARSTAN-chronology development with statistical analysis (users manual for program ARSTAN). Laboratory of Tree-Ring Research. University of Arizona, USA
D´Arrigo R, Davi N, Jacoby G, Wilson R, Wiles G (2014) Dendroclimatic studies: trees growth and climate change in northern forest. American Geophysical Union, Canada
Denk T, Grimm GW (2009) The biogeographic history of beech trees. Rev Palaeobot Palynol 158:83–100
Dittmar C, Elling W (2007) Dendroecological investigation of the vitality of Common Beech (Fagus sylvatica L.) in mixed mountain forests of the Northern Alps (South Bavaria). Dendrochronologia 2:37–56
Drobyshev I, Övergaard R, Saygin I, Niklasson M, Hickler T, Karlsson M, Sykes MT (2010) Masting behaviour and dendrochronology of European beech (Fagus sylvatica L.) in southern Sweden. For Ecol Manag 259:2160–2170
Drobyshev I, Niklasson M, Mazerolle MJ, Bergeron Y (2014) Reconstruction of a 253-year long mast record of European beech reveals its association with large scale temperature variability and no long-term trend in mast frequencies. Agric For Meteorol 192–193:9–17
Ehnis DE (1981) Fagus mexicana Martínez: su ecología e importancia. B. Sc. Thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City
Eller CB, Barros FV, Bittencourt PRL, Rowland L, Mencuccini M, Oliveira RS (2017) Xylem hidraulic safety and construction costs determine tropical tree growth. Plant Cell Environ 2018:1–15
Eşen D (2000) Ecology and control of Rhododendron (Rhododendron ponticum L.) in Turkish eastern beech (Fagus orientalis Lipsky) forest. Doctoral thesis. Virginia Polytechnic Institute and State University, Blacksburg, Virginia, USA
Esperón-Rodríguez M, Barradas VL (2015) Comparing environmental vulnerability in the montane cloud forest of eastern Mexico: a vulnerability index. Ecol Indic 52:300–310
Etemad V, Sefidi K (2017) Seed production and masting behaviour in Oriental beech (Fagus orientalis Lipsky) forests of northern Iran. Forest Ideas 23:65–76
Fang J, Lechowicz MJ (2006) Climatic limits for the present distribution of beech (Fagus L.) species in the world. J Biogeogr 33:1804–1819
FAO (2015) Global forest resources assessment 2015: how are the world´s forest changing? Food Agriculture Organization of the United Nations, Rome
FAO-UNESCO (1988) Soil map of the world. Revised legend. World soil resources report 60. FAO-UNESCO, Rome
Fletcher MS (2015) Mast seeding and the El Niño-Southern Oscillation: a long-term relationship? Plant Ecol 216:527–533
Fonti P, von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gärtner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53
Fritts HC (1976) Tree rings and climate. Academic Press, London
García E (1988) Modificaciones al sistema de clasificación climática de Köppen, México, Offset Larios. Mexico City
García-González I, Fonti P (2008) Ensuring a representative sample of earlywood vessels for dendroclimatological studies: an example from two ring-porous species. Trees 22:237–244
Gareca EE, Fernández M, Stanton S (2010) Dendrochronological investigation of the high Andean tree species Polylepis besseri and implications for management and conservation. Biodivers Conserv 19:1839–1851
Génova M, Moya P (2012) Dendroecological analysis of relict pine forests in the center of the Iberian Peninsula. Biodivers Conserv 21:2949–2965
Godínez-Ibarra O, Ángeles-Pérez G, López-Mata L, García-Moya E, Valdez-Hernández JV, Santos-Posadas H, Trinidad-Santos A (2007) Lluvia de semillas y emergencia de plántulas de Fagus grandifolia subsp. mexicana en La Mojonera, Hidalgo, México. Rev Mex Biodivers 78:117–128
González-Espinosa M, Meave JA, Lorea-Hernández FG, Ibarra-Manríquez G, Newton AC (2011) The Red List of Mexican cloud forest trees. Fauna & Flora International (FFI), Cambridge
González-González BD, Rozas V, García-González I (2013) Early vessels of the sub-Meditterranean oak Quercus pyrenaica have greater plasticity and sensitivity than those of the temperate Q. petrae at the Atlantic-Mediterranean boundary. Trees 28:237–252
Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree Ring Res 57:205–221
Gual-Díaz M, Rendón-Correa A (2014) Bosques mesófilos de montaña de México: diversidad, ecología y manejo. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico City
Hacket-Pain AJ, Friend AD, Lageard JGA, Thomas PA (2015) The influence of masting phenomenon on growth-climate relationships in trees: explaining the influence of previous summers´ climate on ring width. Tree Physiol 35:319–330
Harper JL (1977) Population biology of plants. Academic Press, London
Helama S, Lindholm M, Timonen M, Eronen M (2004) Detection of climate signal in dendrochronological data analysis: a comparison of tree-ring standardization methods. Theor Appl Climatol 79:239–254
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43:69–78
Hukusima T, Matsui T, Nishio T, Pignatti S, Yang L, Lu SY et al (2013) Phytosociology of the beech (Fagus) forest in East Asia. Springer, Heidelberg
Kabeya D, Inagaki Y, Noguchi K, Han Q (2017) Growth rate reduction causes a decline in the annual incremental trunk growth in masting Fagus crenata trees. Tree Physiol 37:1444–1452
Kelly D (1994) The evolutionary ecology of mast seeding. Trees 9:465–470
Kenkel NC, Orlóci L (1986) Applying metric and nonmetric multidimensional scaling to ecological studies: some new results. Ecology 67:919–928
Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi
Kon H, Noda T (2007) Experimental investigation on weather cues for mast seeding of Fagus crenata. Ecol Res 22:802–806
Latte N, Lebourgeois F, Claessens H (2015) Increased tree-growth synchronization of beech (Fagus sylvatica L.) in response to climate change in northwestern Europe. Dendrochronologia 33:69–77
Lemoine N, Sheffield J, Dukes JS, Knapp AK, Smith MD (2016) Terrestrial precipitation analysis (TPA): a resource for characterizing long-term precipitation regimes and extremes. Methods Ecol Evol 7:1396–1401
Manos PS, Stanford AM (2001) The historical biogeography of Fagaceae: tracking the tertiary history of temperate and subtropical forests of the northern hemisphere. Int J Plant Sci 162:S77–S93
Matyas V (1965) Some ecological factors affecting the periodicity of fruit in oak and beech. Erdesz Kutatas Budapest 61:99–121 (in Hungarian with German summary)
Ming-Lee T, Markowitz EM, Howe PD, Ko CY, Leiserowitz AAA (2015) Predictors of public climate change awareness and risk perception around the world. Nat Clim Change 5:1014–1020
Norton DA, Kelly D (1988) Mast seeding over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale. Funct Ecol 2:399–408
Noyer E, Lachenbruch B, Dlouhá J, Collet C, Ruelle J, Ningre F, Fournier (2017) Xylem traits in European beech (Fagus sylvatica L.) display a large plasticity in response to canopy release. Ann For Sci 76:46
Oksanen J, Blanchet FG, Kindt R, Legendre P, Michin PR, Hara RBO´, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) Vegan: community ecology package. R package version 2.3-3. http://cran.r-project.org. Accessed 20 Nov 2016
Övergaard R, Gemmel P, Karlsson M (2007) Effects of weather conditions on mast year frequency in beech (Fagus sylvatica L.) in Sweden. Forestry 80:555–565
Pearse IS, Koenig WD, Kelly D (2016) Mechanisms of mast seeding resources, weather, cues, and selection. New Phytol 212:546–562
Pérez-Rodríguez PM (1999) Las hayas de México, monografía de Fagus grandifolia spp. mexicana. Universidad Autónoma de Chapingo, Chapingo, Mexico City
Peters R (1992) Ecology of beech forests in the northern Hemisphere. Doctoral Thesis, Wageningen Agricultural University, Wageningen, Germany
Peters R (1995) Architecture and development of Mexican beech forest. Vegetation science in forestry. In: Box EO, Peet RK, Masuzawa T, Yamada I, Fujiwara K, Maycock PF (eds) Vegetation science in forestry. Kluwer Academic Publishers, Dordrecht, pp 325–343
Piovensan G, Adams JM (2005) The evolutionary ecology of masting: does the environmental prediction hypothesis also have a role in mesic temperate forests? Ecol Res 20:739–743
Ponce-Reyes R, Reynoso-Rosales VH, Watson JEM, Van Der Wal J, Fuller RA, Pressey RL, Possingham HP (2012) Vulnerability of cloud forest reserves in Mexico to climate change. Nat Clim Change 2:448–452
Pourtahmasi K, Lotfiomran N, Bräuning A, Parsapajouh D (2011) Tree-ring width and vessel characteristics of Oriental beech (Fagus orientalis) along an altitudinal gradient in the Caspian forests, Northern Iran. IAWA J 32:461–473
Price MF, Gratzer G, Duguma LA, Kohler T, Maselli D, Rosalaura R (2011) Mountain forests in a changing world-realizing values, addressing challenges. FAO/MPS and SDC, Rome
Rehm EM, Olivas P, Stroud J, Feeley KJ (2015) Losing your edge: climate change and the conservation value of range-edge populations. Ecol Evol 5:4315–4326
Rinn F (2003) TSAP-Win. Time series analysis and presentation for dendrochronology and related applications for Microsoft Windows, version 4.64. http://www.rinntech.de/content/view/17/48/lang,english/index.html. Accessed 15 Dec 2016
Rita A, Cherubini P, Leonardi S, Todaro L, Borghetti M (2015) Functional adjustments of xylem anatomy to climatic variability: insights from long-term Ilex aquifolium tree-ring series. Tree Physiol 35:817–828
Rodríguez-Ramírez EC, Sánchez-González A, Ángeles-Pérez G (2013) Current distribution and coverage of Mexican beech forests Fagus grandifolia subsp. mexicana in Mexico. Endanger Species Res 20:205–216
Rodríguez-Ramírez EC, Sánchez-González A, Ángeles-Pérez G (2016) Relationship between vegetation structure and microenvironment in Fagus grandifolia subsp. mexicana forest relicts in Mexico. J Plant Ecol 138:1–11
Rodríguez-Ramírez EC, Luna-Vega I, Rozas V (2018) Tree-ring research of Mexican beech (Fagus grandifolia subsp. mexicana) a relict tree endemic to eastern Mexico. Tree Ring Res 74:1
Rossi L, Sebastiani L, Tognetti R, d´Andria R, Morelli G, Cherubini P (2013) Tree-ring wood anatomy and stable isotopes show structural and functional adjustments in olive trees under different water availability. Plant Soil 372:567–579
Rozas V (2001) Detecting the impact of climate and disturbances on tree-rings of Fagus sylvatica L. and Quercus robur L. in a lowland forest in Cantabria, Northern Spain. Ann For Sci 58:237–251
Rozas V, Camarero JJ, Sangüesa-Barreda G, Souto M, García-González I (2015) Summer drought and ENSO-related cloudiness distinctly drive Fagus sylvatica growth near the species rear-edge in norther Spain. Agric For Meteorol 201:153–164
Rozas V, Le Quesne C, Muñoz A, Puchi P (2016) Climate and growth of Podocarpus salignus in Valdivia. Chile Dendrobiol 76:3–11
Rzedowski J (2015) Catálogo preliminar de las especies de árboles silvestres de la Sierra Madre Oriental. In: Flora del Bajío y de regiones adyacentes, fascículo complementario XXX. Instituto de Ecología. A.C. Centro Regional del Bajío Pátzcuaro, Michoacán, Mexico City
Sass U, Eckstein D (1995) The variability of vessel size in beech (Fagus sylvatica L.) and its ecophysiological interpretation. Trees 9:247–252
Sawada H, Kaji M, Oomura K, Igarashi Y (2008) Influences of mast seedling on tree growth dynamics of Fagus crenata and Fagus japonica in central Honshu, Japan. J Jpn For Soc 90:129–136
Schoene DHF, Bernier PY (2012) Adapting forestry and forest to climate change: a challenge to change the paradigm. For Policy Econ 24:12–19
Schweingruber FH (1996) Tree ring and environment: dendroecology. Paul Haupt AG Berne, Switzerland
SEMARNAT, Secretaría del Medio Ambiente y Recursos Naturales (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010. Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación. Segunda Sección, México, Distrito Federal [online]. http://www.profepa.gob.mx/innovaportal/file/435/1/NOM_059_SEMARNAT_2010.pdf. Accessed 06 Apr 2016
Speer JH (2001) Oak mast history from dendrochronology: a new technique demonstrated in the southern Appalachian region. Dissertation, University of Tennessee, Knoxville, USA
Speer JH (2010) Fundamentals of tree ring research. University of Arizona Press, Tucson
Speer JH, Bräuning A, Zhang Q, Pourtahmasi K, Gaire NP, Dawadi B et al (2016) Pinus roxburghii stand dynamics at a heavily impacted site in Nepal: research through an educational fieldweek. Dendrochronologia 41:2–9
Stokes MA, Smiley TL (1968) An introduction to tree-ring dating. University of Chicago Press, Chicago
Suzuki W, Osumi K, Masaki T (2005) Mast seeding and its spatial scale in Fagus crenata in northern Japan. For Ecol Manag 205:105–116
Téllez-Valdés O, Dávila-Aranda P, Lira-Saade R (2006) The effects of climate change on the long-term conservation of Fagus grandifolia var. mexicana, an important species of the cloud forest in eastern Mexico. Biodivers Conserv 15:1095–1107
Tinoco-Rueda JA, Toledo-Medrano ML, Carrillo-Negrete IJ, Monterroso-Rivas I (2009) Clima y variabilidad climática en los municipios de Hidalgo con presencia de bosque mesófilo de montaña. In: Monterroso-Rivas AJ (ed) El bosque mesófilo en el estado de Hidalgo. Perspectiva ecológica frente al cambio climático. Universidad Autónoma Chapingo, Mexico City, pp 71–98
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin
Vacchiano G, Hacket-Pain A, Turco M, Motta R, Maringer J, Conedera M, Drobyshev I, Ascoli D (2016) Spatial patterns and broad-scale weather cues of beech mast seeding in Europe. New Phytol 215:595–608
Venegas-González A, von Arx G, Chagas MP, Filho MT (2015) Plasticity in xylem anatomical traits of two tropical species in response to intra-seasonal climate variability. Trees 29:423–435
von Arx G, Kueffer C, Fonti P (2013) Quantifying plasticity in vessel grouping added value from the image analysis tool Roxas. IAWA J 34:433–445
Wason JW, Dovciak M, Beier CM, Battles JJ (2017) Tree growth is more sensitive than species distributions to recent changes in climate and acidic deposition in the northeastern United States. J Appl Ecol 54:1648–1657
Webster GL (1995) The panorama of Neotropical cloud forest. In: Churchill SP, Balslev H, Forero E, Luteyn JL (eds) Biodiversity and conservation of Neotropical Montane Forests. The New York Botanical Garden, New York, pp 53–57
Williams-Linera G, Rowden A, Newton AC (2002) Distribution and stand characteristics of relict populations of Mexican beech (Fagus grandifolia var. mexicana). Biol Cons 109:27–36
Wood SN (2000) Modelling and smoothing parameter estimation with multiple quadratic penalties. J R Stat Soc Ser B 62:413–428
Yin J, Fridley JD, Smith MS, Bauerle TL (2016) Xylem vessel traits predict the leaf phenology of native and non-native understorey species of temperate deciduous forests. Funct Ecol 30:206–214
Acknowledgements
We wish to thank Osvaldo Franco-Ramos and Lorenzo Vázquez-Selem for their help with tree-ring measurements and for lending the necessary equipment; Susana Guzmán Gómez and María del Carmen Loyola Blanco (Laboratorio de Microscopía y Fotografía de la Biodiversidad II, Instituto de Biología, UNAM) for technical assistance with the digital photographs; Othón Alcántara-Ayala and Rodrigo Ortega García for their support during field work; Ana Paola Martínez-Falcón for assistance with the statistical analyses; Santiago Ramírez-Barahona and Carlos Solís Hay for his critical observations. This research was financed by the project PAPIIT IN223218. The first author thanks the financial support granted by the postdoctoral fellowship DGAPA-UNAM 2015-2016.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by A. Bräuning.
Rights and permissions
About this article
Cite this article
Rodríguez-Ramírez, E.C., Terrazas, T. & Luna-Vega, I. The influence of climate on the masting behavior of Mexican beech: growth rings and xylem anatomy. Trees 33, 23–35 (2019). https://doi.org/10.1007/s00468-018-1755-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-018-1755-3