Ecological Correlates of Ex Situ Seed Longevity: a Comparative Study on 195 Species

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Ecological Correlates of Ex Situ Seed Longevity: a Comparative Study on 195 Species Annals of Botany 104: 57–69, 2009 doi:10.1093/aob/mcp082, available online at www.aob.oxfordjournals.org Ecological correlates of ex situ seed longevity: a comparative study on 195 species Robin J. Probert*, Matthew I. Daws† and Fiona R. Hay Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, UK Received: 1 January 2009 Returned for revision: 17 February 2009 Accepted: 9 March 2009 Published electronically: 9 April 2009 † Background and Aims Extended seed longevity in the dry state is the basis for the ex situ conservation of ‘ortho- dox’ seeds. However, even under identical storage conditions there is wide variation in seed life-span between species. Here, the effects of seed traits and environmental conditions at the site of collection on seed longevity is explored for195 wild species from 71 families from environments ranging from cold deserts to tropical forests. Downloaded from † Methods Seeds were rapidly aged at elevated temperature and relative humidity (either 458C and 60% RH or 608C and 60% RH) and regularly sampled for germination. The time taken in storage for viability to fall to 50% ( p50) was determined using Probit analysis and used as a measure of relative seed longevity between species. † Key Results Across species, p50 at 458C and 60% RH varied from 0.1 d to 771 d. Endospermic seeds were, in general, shorter lived than non-endospermic seeds and seeds from hot, dry environments were longer lived than those from cool, wet conditions. These relationships remained significant when controlling for the effects of phy- http://aob.oxfordjournals.org/ logenetic relatedness using phylogenetically independent contrasts. Seed mass and oil content were not correlated with p50. † Conclusions The data suggest that the endospermic seeds of early angiosperms which evolved in forest under- storey habitats are short-lived. Extended longevity presumably evolved as a response to climatic change or the invasion of drier areas. The apparent short-lived nature of endospermic seeds from cool wet environments may have implications for re-collection and re-testing strategies in ex situ conservation. Key words: Gene banks, seed ageing, seed longevity, taxonomic trends, climate, seed structure. at Universidad Veracruzana on December 7, 2012 INTRODUCTION to 50% between the shortest (Bromus sitchensis; 7 years) and longest lived accessions (Trifolium campestre; 633 years). The fact that seeds of most species can be dried and stored However, there is already evidence that some species from year-to-year has been exploited since the beginning of produce seeds with much shorter longevity in dry storage. agriculture. Indeed, the ability of many orthodox seeds For example, seeds (with high initial viability) of Anemone (sensu Roberts, 1973) to remain viable for tens or hundreds nemorosa are predicted to survive ,1 year under seed bank of years in dry storage (Walters et al., 2005; Daws et al., storage conditions (Ali et al., 2007). As there is an increasing 2007), means that they also provide a convenient vehicle for aspiration to conserve seeds from wild plant species (Target the long-term ex situ conservation of plant germplasm. VIII of the Global Strategy for Plant Conservation; SCBD, The longevity of seeds held in dry storage is mainly deter- 2006), it is likely that more species will be found whose mined by seed moisture content and storage temperature, seeds have a similarly short life-span. with life-span increasing predictably with decreasing tempera- Understanding species differences in seed longevity is there- ture and moisture content (Harrington, 1963, 1972; Ellis and fore crucial to the effective management of seed conservation Roberts, 1980). However, there are also wide inherent differ- collections because it underpins the selection of viability ences in seed longevity between species (Harrington, 1972; re-test intervals and hence regeneration or re-collection strat- Priestley et al., 1985). For example, using the improved seed egies. It is particularly critical for collections of wild plant viability equations (derived from rapid ageing experiments at species where, due to the genetic heterogeneity of wild plant elevated temperatures and moisture contents; Ellis and populations, any significant decline in viability will result in Roberts, 1980), the predicted time for viability to decline the loss of genotypes from the accession (Walters, 2003). from 97.7% to 84.1% for seeds stored under gene-bank con- However, species-specific constants for the improved viability ditions (2208C after equilibration at 15% RH, 158C) ranges equations are only available for approx. 56 species (Liu et al., from approx. 30 years for Ulmus carpinifolia to approx. 2008) the majority of which are temperate species of agricul- 6000 years for Sorghum bicolor (Liu et al., 2008). Similarly, tural importance. Generating constants is time consuming and using the Avrami equation to model data from re-testing of involves the expenditure of tens-of-thousands of seeds per 41 847 seed accessions from 276 species stored at the USDA species. Even if the universal values for the temperature coef- National Center for Genetic Resources Preservation ficients (Dickie et al., 1990) are accepted, carrying out the (NCGRP), Walters et al. (2005) predicted that there would rapid ageing experiments needed to determine the other two be a difference of 626 years in the time for viability to fall parameters would still require thousands of seeds. Thus, species constants are unlikely ever to be experimentally deter- * For correspondence. E-mail [email protected] †Present address: EWL Sciences Pty Ltd, GPO Box 518, Darwin, NT 0800, mined for the majority of plant species. Consequently, predic- Australia. tions of seed longevity in gene-bank storage for threatened # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 58 Probert et al. — Ecological correlates of ex situ seed longevity wild plant species are problematic. An alternative approach to addition, since performance at sub-zero temperatures has to actually determining longevity for individual species is to be extrapolated from rapid ageing conditions, we test identify reliable and robust correlates of longevity and use whether our ageing data correlates with long-term (20-year) these to develop general predictive models (Daws et al., 2006). storage data for species held under gene-bank conditions. A number of studies have reported potential correlates of Specifically, the following hypotheses are tested with the seed longevity in dry storage including seed mass, oil aim of developing a predictive model for seed longevity: (1) content, carbohydrate composition, taxonomy and climate among seed traits, seed mass, oil content and RES will not (e.g. Horbowicz and Obendorf, 1994; Priestley, 1986; be related to seed longevity; (2) climatic parameters (mean Pritchard and Dickie, 2003; Walters et al., 2005). However, annual temperature and total annual rainfall) will not be a purported link between high oil content and short storage related to seed longevity. In comparative analyses, species life-span has not been supported by recent analyses are not statistically independent, as demonstrated by Walters (Pritchard and Dickie, 2003; Walters et al., 2005; Bird, 2006). et al. (2005) for seed longevity. Therefore, not only will cross- Seed size may be used as a predictor of persistence in the species analyses be conducted but also phylogenetically inde- natural environment, with small seeds generally showing pendent contrasts will be conducted to test for an evolutionary greater persistence in the soil seed bank compared with association between the variables of interest and seed storage Downloaded from larger seeds (Thompson et al., 1993; Funes et al., 1999; life-span. Cerabolini et al., 2003; Peco et al., 2003). It might be expected that seeds showing greater persistence in the soil would be long-lived in dry storage. This is supported by reports of a MATERIALS AND METHODS positive correlation between seed longevity measured in the Species selection http://aob.oxfordjournals.org/ laboratory under controlled (Long et al., 2008) or uncontrolled (Bekker et al., 2003) conditions and seed persistence in the High viability collections (85% germination) of 195 species soil. However, no such correlation was found when seed long- with known germination requirements were identified from evity under seed bank conditions was compared with seed per- conservation collections held at the Millennium Seed Bank sistence in soil (Walters et al., 2005), possibly because the under international gene bank standard conditions of 15% stresses and protective mechanisms involved in conferring per- RH and 2208C (FAO/IPGRI, 1994) for between 2 and 35 sistence in the soil are different to the stresses and protective years (Table 1). Species were selected to give broad taxonomic mechanisms that make seeds resistant to ageing in long-term and geographic coverage and were only included if seed long- dry storage at low temperatures. evity characteristics had not been studied previously. They rep- at Universidad Veracruzana on December 7, 2012 The most significant advance in understanding the under- resent a range of orders (30) and families (71), from 658N lying factors influencing seed longevity in dry storage comes (Finland) to 508S (Chile) and 1738E (New Zealand) to from the analysis of the NCGRP data. Walters et al. (2005) 1258W (Canada). suggested both a taxonomic and climatic component to inter- specific differences in longevity. Thus, seeds from some Ageing protocol families were inherently short lived (e.g. Apiaceae, Brassicaceae) and others long-lived (e.g. Malvaceae and Ageing experiments on samples from the targeted collec- Chenopodiaceae) and species originating from cool, temperate tions were carried out between 2001 and 2006. At the outset, climates tended to produce seeds with short life-spans and all seed samples were aged according to a standardized proto- those from warm, arid environments seeds with long life- col (Davies and Probert, 2004).
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