Declining fruit production before death in a widely distributed tree species, Sorbus aucuparia L.
Abstract
Key message
Trees are commonly thought to increase their seed production before death. We tested this terminal investment hypothesis using long-term data on rowan trees ( Sorbus aucuparia ) and found no support. Rather, seed production declined significantly before death, which points to the potential detrimental effects of reproductive senescence on regeneration in stands of old trees.
Context
Aging poses a fundamental challenge for long-lived organisms. As mortality changes with with age due to actuarial senescence, reproductive senescence may also lead to declines in fertility. However, life history theory predicts that reproductive investment should increase before mortality to maximize lifetime reproductive success, a phenomenon termed terminal investment.
Aims
To date, it is unclear whether long-lived, indeterminantly growing trees experience reproductive senescence or display terminal investment.
Methods
We investigated fruit production of rowan (Sorbus aucuparia L.), widely distributed trees that live up to 150 years, as they approached death.
Results
In our study population in Poland’s Carpathian Mountains, 79 trees that died produced up to 20% fewer fruits in the years before their demise compared to 199 surviving trees of the same population.
Conclusion
The pattern of reproductive investment in S. aucuparia is suggestive of age-independent reproductive senescence rather than terminal investment. These findings highlight that the understanding of the generality of life history strategies across diverse taxa of perennial plants is still in its infancy.
Keywords
Reproductive trade-offs Fruit production Senescence Sorbus aucuparia Terminal investment RosaceaeNotes
Funding information
This work was supported by the US National Science Foundation (grant number DEB-1256394 to W.D.K.), Polish National Science Foundation (Sonatina grant number 2017/24/C/NZ8/00151 to M.B.), the Polish State Committee for Scientific Research (grant numbers 6 P04G 045 21, 3 P04G 111 25 to M.Z.), the Polish Ministry of Science and Higher Education (grant number N304 362938 to M.Z.), and the statutory fund of the Institute of Botany of the Polish Academy of Sciences.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
References
- Adler PB, Salguero-Gómez R, Compagnoni A, Hsu JS, Ray-Mukherjee J, Mbeau-Ache C, Franco M (2014) Functional traits explain variation in plant life history strategies. Proc Natl Acad Sci 111:740–745. https://doi.org/10.1073/pnas.1315179111 CrossRefPubMedGoogle Scholar
- Ally DK, Ritland K, Otto SP (2010) Aging in a long-lived clonal tree. PLoS Biol 8:e1000454. https://doi.org/10.1371/journal.pbio.1000454 CrossRefPubMedPubMedCentralGoogle Scholar
- Barringer BC, Koenig WD, Knops JMH (2013) Interrelationships among life-history traits in three California oaks. Oecologia 171:129–139. https://doi.org/10.1007/s00442-012-2386-9 CrossRefPubMedGoogle Scholar
- Baudisch A, Salguero-Gómez R, Jones OR, Wrycza T, Mbeau-Ache C, Franco M, Colchero F (2013) The pace and shape of senescence in angiosperms. J Ecol 101:596–606. https://doi.org/10.1111/1365-2745.12084 CrossRefGoogle Scholar
- Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) Modeling zero-inflated count data with glmmTMB. bioRxiv preprint bioRxiv:132753. https://doi.org/10.1101/132753
- Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229. https://doi.org/10.1086/284198 CrossRefGoogle Scholar
- Creighton JC, Heflin ND, Belk MC (2009) Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am Nat 174:673–684. https://doi.org/10.1086/605963 CrossRefPubMedGoogle Scholar
- Fernández-Martínez M, Garbulsky M, Peñuelas J, Peguero G, Espelta JM (2015) Temporal trends in the enhanced vegetation index and spring weather predict seed production in Mediterranean oaks. Plant Ecol 216:1061–1072. https://doi.org/10.1007/s11258-015-0489-1 CrossRefGoogle Scholar
- Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford. https://doi.org/10.5962/bhl.title.27468 CrossRefGoogle Scholar
- Grime JP, Hodgson JG, Hunt R (1988) Comparative plant ecology. A functional approach to common British species. Unwin Hyman, London. https://doi.org/10.1007/978-94-017-1094-7 CrossRefGoogle Scholar
- Hamilton WD (1966) The moulding of senescence by natural selection. J Theor Biol 12:12–45. https://doi.org/10.1016/0022-5193(66)90184-6 CrossRefPubMedGoogle Scholar
- Hammers M, Richardson DS, Burke T, Komdeur J (2012) Age-dependent terminal declines in reproductive output in a wild bird. PLoS One 7:e40413. https://doi.org/10.1371/journal.pone.0040413 CrossRefPubMedPubMedCentralGoogle Scholar
- Hartig F (2018) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.1.6Google Scholar
- Holeksa J, Jaloviar P, Kucbel S, Saniga M, Svoboda M, Szewczyk J, Szwagrzyk J, Zielonka T, Żywiec M (2017) Models of disturbance driven dynamics in the West Carpathian spruce forests. For Ecol Manag 388:79–89. https://doi.org/10.1016/j.foreco.2016.08.026 CrossRefGoogle Scholar
- Iwasa Y, Cohen D (1989) Optimal growth schedule of a perennial plant. Am Nat 133:480–505. https://doi.org/10.1086/284931 CrossRefGoogle Scholar
- Jones OR, Scheuerlein A, Salguero-Gómez R, Camarda CG, Schaible R, Casper BB, Dahlgren JP, Ehrlén J, García MB, Menges ES, Quintana-Ascencio PF (2014) Diversity of ageing across the tree of life. Nature 505:169–173. https://doi.org/10.1038/nature12789 CrossRefPubMedGoogle Scholar
- Kirkwood TB (1987) Immortality of the germ-line versus disposability of the soma. In: Woodhead AD (ed) Evolution of longevity in animals. Springer, Boston, pp 209–218. https://doi.org/10.1007/978-1-4613-1939-9_15 CrossRefGoogle Scholar
- Knops JMH, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proc Natl Acad Sci 104:16982–16985. https://doi.org/10.1073/pnas.0704251104 CrossRefPubMedGoogle Scholar
- Koenig WD, Knops JMH, Carmen WJ, Pesendorfer MB (2017) Testing the terminal investment hypothesis in California oaks. Am Nat 189:564–569. https://doi.org/10.1086/691161 CrossRefPubMedGoogle Scholar
- Kozłowski J (1993) Measuring fitness in life, history studies. Trends Ecol Evol 8:84–85. https://doi.org/10.1016/0169-5347(93)90056-U CrossRefPubMedGoogle Scholar
- Magnusson A, Skaug HJ, Nielsen A, Berg CW, Kristensen K, Maechler M, van Bentham KJ, Bolker BM, Brooks ME (2017) glmmTMB: Generalized linear mixed models using template model builder. R package version 01.3Google Scholar
- Martin JG, Festa-Bianchet M (2011) Age-independent and age-dependent decreases in reproduction of females. Ecol Lett 14:576–581. https://doi.org/10.1111/j.1461-0248.2011.01621.x CrossRefPubMedGoogle Scholar
- Medawar PB (1952) An unsolved problem of biology. H.K. Lewis & Co, LondonGoogle Scholar
- Munné-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220. https://doi.org/10.1016/j.tplants.2008.02.002 CrossRefPubMedGoogle Scholar
- Munné-Bosch S (2015) Senescence: is it universal or not? Trends Plant Sci 20:713–720. https://doi.org/10.1016/j.tplants.2015.07.009 CrossRefPubMedGoogle Scholar
- Pearse IS, Koenig WD, Kelly D (2016) Mechanisms of mast seeding: resources, weather, cues, and selection. New Phytol 212:546–562. https://doi.org/10.1111/nph.14114 CrossRefPubMedGoogle Scholar
- Pedersen BS (1998) Modeling tree mortality in response to short-and long-term environmental stresses. Ecol Model 105:347–351. https://doi.org/10.1016/S0304-3800(97)00162-2 CrossRefGoogle Scholar
- Pesendorfer MB, Koenig WD, Pearse IS, Knops JMH, Funk KA (2016) Individual resource limitation combined with population-wide pollen availability drives masting in the valley oak (Quercus lobata). J Ecol 104:637–645. https://doi.org/10.1111/1365-2745.12554 CrossRefGoogle Scholar
- Pesendorfer MB, Bogdziewicz M, Koenig WD, Ledwoń M, Żywiec M (2018) Data for “Declining fruit production before death in a widely distributed tree, Sorbus aucuparia L.”. V1. FigShare. [Dataset]. https://doi.org/10.6084/m9.figshare.7330052.v1
- R Core Team (2018) R: a language and environment for statistical computing. R software version 3.4.4Google Scholar
- Raspé O, Findlay C, Jacquemart AL (2000) Sorbus aucuparia L. J Ecol 88:910–930. https://doi.org/10.1046/j.1365-2745.2000.00502.x CrossRefGoogle Scholar
- Salguero-Gómez R, Shefferson RP, Hutchings MJ (2013) Plants do not count… or do they? New perspectives on the universality of senescence. J Ecol 101:545–554. https://doi.org/10.1111/1365-2745.12089 CrossRefPubMedPubMedCentralGoogle Scholar
- Salguero-Gómez R, Jones OR, Archer CA, Buckley YM, Che-Castaldo J, Caswell C, Hodgson D, Scheuerlein A, Conde DA, Brinks E, Buhr H (2015) The COMPADRE Plant Matrix Database: an online repository for plant population dynamics. J Ecol 103:202–218. https://doi.org/10.1111/1365-2745.12334 CrossRefGoogle Scholar
- Salguero-Gómez R, Jones OR, Jongejans E, Blomberg SP, Hodgson DJ, Mbeau-Ache C, Zuidema PA, de Kroon H, Buckley YM (2016) Fast–slow continuum and reproductive strategies structure plant life-history variation worldwide. Proc Natl Acad Sci 113:230–235. https://doi.org/10.1073/pnas.1506215112 CrossRefPubMedGoogle Scholar
- Satake A, Bjørnstad ON, Kobro S (2004) Masting and trophic cascades: interplay between rowan trees, apple fruit moth, and their parasitoid in southern Norway. Oikos 104:540–550. https://doi.org/10.1111/j.0030-1299.2004.12694.x CrossRefGoogle Scholar
- Shefferson RP, Roach DA (2013) Longitudinal analysis in Plantago: strength of selection and reverse age analysis reveal age-indeterminate senescence. J Ecol 101:577–584. https://doi.org/10.1111/1365-2745.12079 CrossRefPubMedPubMedCentralGoogle Scholar
- Sletvold N, Ågren J (2015) Climate-dependent costs of reproduction: survival and fecundity costs decline with length of the growing season and summer temperature. Ecol Lett 18:357–364. https://doi.org/10.1111/ele.12417 CrossRefPubMedGoogle Scholar
- Sperens U (1997) Long-term variation in, and effects of fertiliser addition on, flower, fruit and seed production in the tree Sorbus aucuparia (Rosaceae). Ecography 20:521–534. https://doi.org/10.1111/j.1600-0587.1997.tb00421.x CrossRefGoogle Scholar
- Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51:3–47. https://doi.org/10.1086/409052 CrossRefPubMedGoogle Scholar
- Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytol 197:696–711. https://doi.org/10.1111/nph.12047 CrossRefPubMedGoogle Scholar
- Tifferet S, Kruger DJ (2010) The terminal investment hypothesis and age-related differences in female preference for dads vs. cads. Lett Evol Behav Sci 1:27–30. https://doi.org/10.5178/lebs.2010.7 CrossRefGoogle Scholar
- Vacchiano G, Ascoli D, Berzaghi F, Lucas-Borja ME, Caignard T, Collalti A, Mairota P, Palaghianu C, Reyer CP, Sanders TG, Schermer E (2018) Reproducing reproduction: how to simulate mast seeding in forest models. Ecol Model 376:40–53. https://doi.org/10.1016/j.ecolmodel.2018.03.004 CrossRefGoogle Scholar
- Weismann A (1893) The germ-plasm: a theory of heredity. Scribner, New YorkGoogle Scholar
- Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411. https://doi.org/10.1111/j.1558-5646.1957.tb02911.x CrossRefGoogle Scholar
- Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690. https://doi.org/10.1086/282461 CrossRefGoogle Scholar
- Wohlleben P (2016) The hidden life of trees. Greystone, VancouverGoogle Scholar
- Yoccoz NG, Mysterud A, Langvatn R, Stenseth NC (2002) Age- and density-dependent reproductive effort in male red deer. Proc R Soc B Biol Sci 269:1523–1528. https://doi.org/10.1098/rspb.2002.2047 CrossRefGoogle Scholar
- Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology. Springer, New YorkCrossRefGoogle Scholar
- Żywiec M, Ledwoń M (2008) Spatial and temporal patterns of rowan (Sorbus aucuparia L.) regeneration in West Carpathian subalpine spruce forest. Plant Ecol 194:283–291. https://doi.org/10.1007/s11258-007-9291-z CrossRefGoogle Scholar
- Żywiec M, Zielonka T (2013) Does a heavy fruit crop reduce the tree ring increment? Results from a 12-year study in a subalpine zone. Trees 27:1365–1373. https://doi.org/10.1007/s00468-013-0884-y CrossRefGoogle Scholar
- Żywiec M, Holeksa J, Ledwoń M (2012) Population and individual level of masting in a fleshy-fruited tree. Plant Ecol 213:993–1002. https://doi.org/10.1007/s11258-012-0059-8 CrossRefGoogle Scholar
- Żywiec M, Ledwoń M, Holeksa J, Seget S, Łopata B, Fedriani JM (2018) Rare events of massive plant reproductive investment lead to long-term density-dependent reproductive success. J Ecol 106:1307–1318. https://doi.org/10.1111/1365-2745.12896 CrossRefGoogle Scholar