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Reproductive costs in Acer saccharum: exploring size-dependent relations between seed production and branch extension

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Branch extension of Acer saccharum is negatively correlated with seed production, with no independent effect of tree size, consistent with reproductive allocation as the main driver of the age-related decline in tree canopy growth.

Abstract

Life-history theory predicts that reproductive allocation should increase with age and size once plants reach reproductive maturity. This suggests that there may also be a subsequent decline in somatic growth as plants become larger or older. However, few studies have examined how the relationship between branch extension growth and reproduction varies with size or age in the longest-lived plants: trees. Using a mobile lift for canopy access, we retrospectively measured branch extension growth before, during and after two (between 2011 and 2013) Acer saccharum mast events (the synchronous production of many seeds at long intervals), quantifying seed production per internode and internode length. Branch extension was reduced by 24 and 36%, respectively, in 2011 and 2013 relative to non-mast years, consistent with the expectation that increased reproductive allocation comes at the cost of allocation to growth. Internode length decreased from 8 to 3 cm year−1 as seed production increased from zero to 17 seeds year−1; a similar decrease was observed at the whole-tree level using average internode extension rates and seed production per tree. Seed production alone was the most parsimonious predictor of branch extension growth, with no independent effect of tree size, suggesting that it is the increase in reproductive allocation, rather than an increase in tree size per se, that drives the decline in branch extension rates. The slope of the relationship between branch extension and reproduction did not vary with tree size, suggesting that there was no increase in the somatic cost of reproduction with tree size. We also found no evidence for lag effects of reproduction on extension growth in subsequent years. Overall, these results suggest that reproductive allocation assessed at the shoot level increases with tree size and is a major driver of the ontogenetic decline in branch extension growth.

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References

  • Barnard HR, Ryan MG (2003) A test of the hydraulic limitation hypothesis in fast-growing Eucalyptus saligna. Plant Cell Env 26: 1235–1245

    Article  Google Scholar 

  • Bazzaz FA, Ackerly DD, Reekie EG (2000) Reproductive allocation and reproductive effort in plants. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CAB International, Oxford, pp 1–37

    Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Tren Ecol Evol 20:520–526

    Article  Google Scholar 

  • Bond BJ, Ryan MG (2000) Comment on ‘Hydraulic limitation of tree height: a critique’ by Becker, Meinzer & Wullschleger. Funct Ecol 14:137–140

    Article  Google Scholar 

  • Bond BJ, Czarnomski NM, Cooper C et al (2007) Developmental decline in height growth in Douglas-fir. Tree Physio 27: 441–453

    Article  Google Scholar 

  • Bonser SP, Aarssen LW (1994) Plastic allometry in young sugar maple (Acer saccharum): adaptive responses to light availability. Am J Bot 81:400–406

    Article  Google Scholar 

  • Brunner AM, Li JY, DiFazio SP et al (2007) Genetic containment of forest plantations. Tree Gen Geno 3: 75–100

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model Selection and Inference: A Practical Information-Theoretic Approach. Springer-Verlag, New York

    Book  Google Scholar 

  • Choi J, Lorimer CG, Vanderwerker J et al (2001) A crown model for simulating long term stand and gap dynamics in northern hardwood forests. For Ecol Manage 152:235–258

    Article  Google Scholar 

  • Cole WG, Lorimer CG (2005) Probabilities of small-gap capture by sugar maple saplings based on height and crown growth data from felled trees. Can J For Res 35:643–655

    Article  Google Scholar 

  • Despland E, Houle G (1997) Climate influences on growth and reproduction of Pinus banksiana (Pinaceae) at the limit of the species distribution in Eastern North America. Am J Bot 84:928–937

    Article  CAS  PubMed  Google Scholar 

  • Dick JM, Leakey RRB, Jarvis PG (1990) Influence of female cones the vegetative growth of Pinus contorta trees. Tree Physio l6: 151–163

    Article  CAS  Google Scholar 

  • Environment Canada (2004). Canadian Climate Normals 1971–2000. Accessed in 2005.

  • Filewod B, Thomas SC (2014) Impacts of a spring heat wave on canopy processes in a northern hardwood forest. Glob Chan Bio 20: 360–371

    Article  Google Scholar 

  • Fox JF, Stevens GC (1991) Costs of reproduction in a willow: experimental responses vs. natural variation. Ecology 72:1013–1023

    Article  Google Scholar 

  • Genet H, Bréda N, Dufrêne E (2010) Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) using a chronosequence approach. Tree Physio 30: 177–192

    Article  CAS  Google Scholar 

  • Godman RM, Yawney HW, Tubbs CH (1990) Acer saccharum (Marsh.) sugar maple. Silvics of North America. Vol. 2. Hardwoods Agric. Handb. 654 (Burns, Russell M.; Honkala, Barbara H., technical coordinators), Washington DC, U.S. Department of Agriculture, Forest Service, pp 78–91

    Google Scholar 

  • Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. Tren Ecolog Evol Res 11: 378–382

    Article  CAS  Google Scholar 

  • Gross HL (1972) Crown deterioration and reduced growth associated with excessive seed production by birch. Can J Bot 50:2431–2437

    Article  Google Scholar 

  • Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Tren Ecol Evol 22:80–86

    Article  Google Scholar 

  • Hibbs DE (1982) Gap dynamics in a hemlock-hardwood forest. Can J For Res 12:522–527

    Article  Google Scholar 

  • Hossain SMY, Caspersen JP (2012) In-situ measurement of twig dieback and regrowth in mature Acer saccharum trees. For Ecol Manage, 270: 183–188

    Article  Google Scholar 

  • Iwasa Y (2000) Dynamic optimization of plant growth. Evol Ecol Res 2:427–455

    Google Scholar 

  • Iwasa Y, Cohen D (1989) Optimal growth schedule of a perennial plant. Am Nat 133:480–505

    Article  Google Scholar 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why how where? Ann Rev Ecol Sys 33:427–447

    Article  Google Scholar 

  • King D, Roughgarden J (1982) Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theor Pop Biol 21: 1–16

    Article  Google Scholar 

  • Knops JMH, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proc the Nat Aca Sci, USA 104: 16982–16985

  • Koch GW, Sillett SC, Jennings GM et al (2004) The limits to tree height. Nature 428:851–854

    Article  CAS  PubMed  Google Scholar 

  • Kozlowski TT, Clausen JJ (1966) Shoot growth characteristics of heterophyllous woody plants. Can J Bot 44:827–843

    Article  Google Scholar 

  • Kutsch WL, Wirth C, Kattge K et al (2009) Ecophysiological characteristics of mature trees and stands – consequences for old-growth forest productivity. In: Wirth C, Gleixner G, Heimann M (eds) Old growth forests: function, value and fate. Springer, Berlin, pp 57–69

    Chapter  Google Scholar 

  • Loehle C (1988) Tree life-history strategies: the role of defenses. Can J For Res 18:209–222

    Article  Google Scholar 

  • Luzadis VA, Gossett ER (1996) Sugar Maple. In: Lassoie, JP, Luzadis VA, Grover DW (eds) Forest Trees of the Northeast, Cooperative Extension Bulletin 235, Cornell Media Services, University of Cornell, pp 157–166

  • McGee CE (1986) Budbreak for Twenty-Three Upland Hardwoods Compared Under Forest Canopies and in Recent Clearcuts. For Sci 32(4): 924–935

    Google Scholar 

  • Mendez M, Obeso JR (1993) Size-dependent reproductive and vegetative allocation in Arum italicum (Araceae). Can J Bot 71:309–314

    Article  Google Scholar 

  • Monks A, Kelly D (2006) Testing the resource-matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae). Aust Ecol 31: 366–375

    Article  Google Scholar 

  • Mouradov A, Teasdale RD (1999) Genetic engineering of reproductive incompetence in radiata pine. Protoplasma 208(1–4):13–17

    Article  CAS  Google Scholar 

  • 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. Func Ecol 2: 399–408

    Article  Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phyto 155: 321–348

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Purves DW, Lichstein JW, Pacala SW (2007) Crown plasticity and competition for canopy space: a new spatially implicit model parameterized for 250 North American tree species. PLoS One 2:e870

    Article  PubMed  PubMed Central  Google Scholar 

  • Reekie EG, Bazzaz FA (1992) Cost of reproduction as reduced growth in genotypes of two congeneric species with contrasting life histories. Oecologia 90:21–26

    Article  CAS  PubMed  Google Scholar 

  • Renner SS, Beenken L, Grimm GW et al (2007) The evolution of dioecy, heterodichogamy, and labile sex expression in Acer. Evolution Int J org Evolution 61:2701–2719

    Article  CAS  Google Scholar 

  • Ryan MG, Binkley D, Fownes JH (1997) Age-related decline in forest productivity: Pattern and Process. Adv Ecol Res 27:214–262

    Google Scholar 

  • Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Env 29: 367–381

    Article  Google Scholar 

  • Sanchez-Humanes B, Sork VL, Espelta JM (2011) Trade-offs between vegetative growth and acorn production in Quercus lobata during a mast year: the relevance of crop size and hierarchical level within the canopy. Oecologia 166:101–110

    Article  PubMed  Google Scholar 

  • Silvertown J, Dodd M (1999) The Demographic Cost of Reproduction and Its Consequences in Balsam Fir (Abies balsamea). Am Nat 154:321–332

    Article  CAS  PubMed  Google Scholar 

  • Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Ann Rev Ecol Sys 22:309–334

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Steingraeber DA (1982) Heterophylly and Neoformation of leaves in sugar maple (Acer saccharum). Am J Bot 69(8):1277–1282

    Article  Google Scholar 

  • Stephenson NL et al (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507:90–93

    Article  CAS  PubMed  Google Scholar 

  • Strauss SH, Rottmann WH, Brunner AM et al (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26

    Article  CAS  Google Scholar 

  • Tappeiner JC (1969) Effect of cone production on branch, needle, and xylem ring growth of Sierra Nevada Douglas-fir. For Sci 15: 171–174

    Google Scholar 

  • Thomas SC (1996) Reproductive allometry in Malaysian rain forest trees: biomechanics versus optimal allocation. Evol Ecol 10:517–530

    Article  Google Scholar 

  • Thomas SC (2010) Photosynthetic capacity peaks at intermediate size in temperate deciduous trees. Tree Physio 30: 555–573

    Article  Google Scholar 

  • Thomas SC (2011) Age-related changes in tree growth and functional biology: the role of reproduction. In: Meinzer FC, Dawson T, Lachenbruch BJ (eds) Invited chapter for Size- and age-related changes in tree structure and function, tree physiology, Springer-Verlag, pp 33–64

  • Thomas SC, Martin AR, Mycroft EE (2015) Tropical trees in a wind-exposed island ecosystem: height-diameter allometry and size at onset of maturity. J Ecol 103:594–605

    Article  Google Scholar 

  • Thorpe HC, Astrup R, Trowbridge A et al (2010) Competition and tree crowns: a neighborhood analysis of three boreal tree species. For Ecol Manage 259: 1586–1596

    Article  Google Scholar 

  • Tuomi J, Neimela P, Mannila R (1982) Resource allocation on dwarf shoots of birch (Betula pendula) – reproduction and leaf growth. New Phyto 91: 483–487

    Article  Google Scholar 

  • United States Department of Agriculture (USDA) (2008) Woody Plant Seed manual. USDA Forest Service, Agriculture Handbook 727

  • Wallace CS, Rundel PW (1979) Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia 44:34–39

    Article  PubMed  Google Scholar 

  • Watson GW, Himelick EB, Smiley ET (1986) Twig growth of eight species of shade trees following transplanting. J Arbori 12(10):241–245

    Google Scholar 

  • Weiner J, Thomas SC (2001) The nature of tree growth and the age-related decline in forest productivity. Oikos 94:374–376

    Article  Google Scholar 

  • Wheelwright NT, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proc Nat Aca Sci USA 101: 8051–8055

    Article  CAS  Google Scholar 

  • Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Env 27: 229–236

    Article  Google Scholar 

  • Woodward A, Silsbee DG, Schreiner EG et al (1993) Influence of climate on radial growth and cone production in subalpine fir (Abies lasiocarpa) and mountain hemlock (Tsuga mertensiana). Can J For Res 24:1133–1143

    Article  Google Scholar 

  • Worley AC, Harder LD (1996) Size-dependent resource allocation and costs of reproduction in Pinguicula vulgaris (Lentibulariaceae). J Ecol 84:195–206

    Article  Google Scholar 

  • Yasumura Y, Hikosaka K, Hirose T (2006) Resource allocation to vegetative and reproductive growth in relation to mast seeding in Fagus crenata. For Ecol Manage 229: 228–233

    Article  Google Scholar 

  • Yoder BJ, Ryan MG, Waring RH et al (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40: 513–527

    Google Scholar 

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Acknowledgements

We thank Haliburton Forest and Wildlife Reserve for their support to conduct this research, Philip Rudz and Lazar Pavlovic for their field assistance, as well as Tomasz Gradowski for providing lift training. We also thank Tat Smith of the University of Toronto and Bill Cole of the MNR, Ontario for their comments on an earlier version of this manuscript.

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Correspondence to Shaik Md. Yousuf Hossain.

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Communicated by M. Knoche.

Appendix 1

Appendix 1

A power analysis was conducted to determine the minimum sample size per tree in order to detect a significant trend. First we pulled out data for the largest and smallest tree, and then resampled with replacement to calculate proportion of statistically significant comparisons by a simple t test (results not shown). This analysis showed that a sample of 3–6 branches would provide one a 10% chance of detecting a significant trend, with an assumed effect size value of 0.5 (coefficient of determination). However, the minimum sample size should have been ~40 to achieve a statistical power of 0.8 (Table 3).

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Hossain, S.M.Y., Caspersen, J.P. & Thomas, S.C. Reproductive costs in Acer saccharum: exploring size-dependent relations between seed production and branch extension. Trees 31, 1179–1188 (2017). https://doi.org/10.1007/s00468-017-1536-4

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