The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise

Biol. Rev. (2014), pp. 000–000. 1doi: 10.1111/brv.12095

The ecophysiology of seed persistence:a mechanistic view of the journeyto germination or demise

Rowena L. Long1,2, Marta J. Gorecki1,2, Michael Renton1,3,∗, John K. Scott3,4,Louise Colville5, Danica E. Goggin1, Lucy E. Commander1,6, David A. Westcott7,Hillary Cherry8 and William E. Finch-Savage9

1School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia2ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia

6009, Australia3CSIRO Ecosystem Sciences and Climate Adaptation Flagship, 147 Underwood Avenue, Floreat, Western Australia 6014, Australia4School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia5Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, U.K.6Kings Park and Botanic Garden, Fraser Avenue, West Perth, Western Australia 6005, Australia7CSIRO Ecosystem Sciences, Maunds Road, Atherton, Queensland 4883, Australia8Pest and Ecological Management Unit, NSW Office of Environment and Heritage, PO Box 1967, Hurstville, New South Wales 1481, Australia9School of Life Sciences, Warwick University, Wellesbourne, Warwick CV35 9EF, U.K.

ABSTRACT

Seed persistence is the survival of seeds in the environment once they have reached maturity. Seed persistence allowsa species, population or genotype to survive long after the death of parent plants, thus distributing genetic diversitythrough time. The ability to predict seed persistence accurately is critical to inform long-term weed management andflora rehabilitation programs, as well as to allow a greater understanding of plant community dynamics. Indeed, each ofthe 420000 seed-bearing plant species has a unique set of seed characteristics that determine its propensity to develop apersistent soil seed bank. The duration of seed persistence varies among species and populations, and depends on thephysical and physiological characteristics of seeds and how they are affected by the biotic and abiotic environment. Anintegrated understanding of the ecophysiological mechanisms of seed persistence is essential if we are to improve ourability to predict how long seeds can survive in soils, both now and under future climatic conditions. In this review wepresent an holistic overview of the seed, species, climate, soil, and other site factors that contribute mechanistically toseed persistence, incorporating physiological, biochemical and ecological perspectives. We focus on current knowledgeof the seed and species traits that influence seed longevity under ex situ controlled storage conditions, and explore howthis inherent longevity is moderated by changeable biotic and abiotic conditions in situ, both before and after seeds aredispersed. We argue that the persistence of a given seed population in any environment depends on its resistance toexiting the seed bank via germination or death, and on its exposure to environmental conditions that are conducive tothose fates. By synthesising knowledge of how the environment affects seeds to determine when and how they leavethe soil seed bank into a resistance–exposure model, we provide a new framework for developing experimental andmodelling approaches to predict how long seeds will persist in a range of environments.

Key words: pre-dispersal, post-dispersal, predation, seed ageing, seed decay, seed defence, seed dispersal, seed dormancy,seed longevity, seed persistence.

* Author for correspondence (Tel: +61 8 64881959; E-mail: [email protected]).

Biological Reviews (2014) 000–000 © 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society

2 Rowena L. Long and others

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3(1) Aims of this review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3(2) Significance of seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

(a) Ecological significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3(b) Restoration and conservation management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4(c) Weed management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5(d ) Agricultural management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

II. Seed characteristics that influence persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6(1) Seed dormancy and germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

(a) Conditions that alleviate dormancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7(b) Dormancy cycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8(c) Germination conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

(2) Inherent seed longevity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(a) Desiccation tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(b) Sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(c) Seed lipids and membrane integrity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(d ) Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10(e) Key antioxidants: capacity to resist deterioration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10(f ) Resistance to genetic degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

(3) Seed characteristics related to dispersal, defence and germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11(a) Seed size and embryo-endosperm proportions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11(b) Seed nutritive value for predators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11(c) Characteristics of seed coats and other surrounding tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11(d ) Seed appendages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12(e) Seed exudates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12(f ) Symbioses with endophytic microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

III. Species characteristics related to seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12(1) Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13(2) Life history and reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

(a) Life history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13(b) Reproductive syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13(c) Seed production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

(3) Genetic diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13(4) Phenotypic plasticity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14(5) Species geography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14(6) Alternative seed storage location: the canopy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

IV. Pre-dispersal environmental factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15(1) Abiotic influences of the parental environment on seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15(2) Biotic stress in the parental environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

V. Post-dispersal environmental factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16(1) Climatic factors affecting seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

(a) Temperature, rainfall and humidity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16(b) Wet-dry cycles: a special case . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16(c) Future climates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

(2) Soil factors affecting seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17(a) Physical . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17(b) Chemical . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17(c) Gaseous environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17(d ) Biological . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

(3) Other site-related environmental factors affecting persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18(a) Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18(b) Disturbance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18(c) Burial depth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18(d ) Toxic and dormancy-breaking chemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18(e) Modification by dispersal agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19(f ) Post-dispersal predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

VI. Integrating available knowledge into a predictive model of seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20(1) The resistance–exposure model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20


The ecophysiology of seed persistence 3

(2) Applications for improved predictive modelling of seed persistence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

VIII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

I. INTRODUCTION

Seed persistence refers to the survival of seeds after theyreach maturity on the parent plant. Ecologically speaking,seed persistence allows plants to disperse their seeds throughtime and to avoid germination in adverse conditions(Cohen, 1966; Venable & Brown, 1988; Ooi, 2012). Inan evolutionary context, delaying seed germination throughtime is a bet-hedging strategy that spreads the risk ofreproductive failure, which is particularly important inunpredictable environments where the risk of dying beforereaching maturity is high (Cohen, 1966). From a humanperspective, seed persistence also enables seeds to be stored exsitu and used in society. Once mature, seeds can persist in thesoil seed bank, in the plant canopy (as in the case of serotiny)or in ex situ storage until they experience one of two fates:germination or death (Fig. 1). Seeds can persist for a very longtime in ex situ storage where conditions are relatively stable,e.g. 2000 years for date seeds (Phoenix dactylifera L.) recoveredfrom an Herodian fortress near the Dead Sea (Sallon et al.,2008) and 151 years for Acacia spp. seeds from Egypt stored inSwedish museums (Leino & Edqvist, 2010). Indeed, purpose-built ex situ seed banks such as Kew’s Millennium SeedBank and the USDA National Plant Germplasm Systemcapitalise on the ability of seeds to survive for long periodsunder optimal storage conditions [−18◦C or −20◦C, andapproximately 15% equilibrium relative humidity (RH)], andhave successfully stored wild and domesticated seeds for over35 years (Walters, Wheeler & Grotenhuis, 2005c; Probert,Daws & Hay, 2009). By contrast, seeds dispersed into thenatural environment encounter dynamic climatic, soil andsite conditions, which results in variable persistence times. InDr Beal’s famous 120-year seed-burial experiment, seeds ofsome species died within 5 years, whilst others persisted forover 100 years (Telewski & Zeevaart, 2002). Thus, from amechanistic perspective, seed persistence is an expression ofnumerous seed characteristics including inherent dormancy,longevity and defence (Fig. 1; see also definitions in Table 1),and how these characteristics are influenced by the seed’simmediate environment (Fig. 2).

(1) Aims of this review

In this review we explore the seed, species and environmentalfactors (including climatic, soil, and other site factors) thatcontribute to seed persistence, incorporating physiological,biochemical and ecological perspectives. There have beenmany studies of seed persistence for particular species andenvironments, and a small number of review papers andbooks that address aspects of seed persistence in the contextof climate change (Walck et al., 2011; Ooi, 2012), weed

management (Gallagher & Fuerst, 2006), or general andevolutionary ecology (Rees, 1996; Baskin & Baskin, 2001;Fenner & Thompson, 2005). However, we are not aware of acomprehensive review that explores the suite of mechanisticseed and environmental factors that influence persistenceand synthesises them into a model to aid future predictionsin a range of environments. To this end we describe theinterplay between the characteristics of seeds and speciesthat confer ‘resistance’ to physiological ageing, germination,predation by animals and microbial decay, and the ‘exposure’to climatic, soil and other site conditions in the pre-dispersaland post-dispersal environment that ultimately determineshow long seeds survive (Fig. 2). Our focus is primarily on seedspersisting in soils, however much can be learnt from, andapplied to, studies of seeds in ex situ storage, which is anotherenvironment with measurable attributes. We propose that aresistance–exposure model can drive future understandingand predictions of seed persistence in any context, andhighlight areas for future research.

(2) Significance of seed persistence

Seed persistence is an important consideration forcommunity ecology, flora restoration programs, and weedand agricultural management, where the relative persistenceof species impacts on the presence and abundance ofplants and therefore influences decisions on how bestto manage them. The persistence of seeds in situ canbe classified as transient, short-lived or long-lived: seedssurviving < 1 year are termed transient or non-persistent,and those surviving ≥ 1 year are termed persistent; often thedistinction between short-lived and long-lived is drawn at 3or 5 years, but this is arbitrary and depends on the contextand application (Thompson et al., 1998; Long et al., 2008).A comprehensive review of persistence classification systemscan be found in Csontos & Tamas (2003).

(a) Ecological significance

Seed persistence allows plant populations to disperse in timeas well as in space, increasing the likelihood that some seedsof a plant’s cohort will encounter favourable germinationand establishment environments. Theoretically, for seeds topersist until conditions are favourable for establishment,parent plants will produce an appropriate volume ofseeds that will exhibit specific adaptations in dormancy,germination, longevity and morphology, reflecting theseasonality and predation or decay risk in the environmentin which the species evolved (see also Dalling et al., 2011). Inenvironments that are either aseasonal or strongly seasonal interms of recruitment opportunities, and are thus predictable,



Fig. 1. Seeds persist until they either germinate or die due to ageing, predation or decay. Seed dormancy, longevity and defenceare key characteristics of seeds that contribute to persistence.

the seed-persistence strategies that are favoured ensurethat seeds germinate under optimal conditions for survival(Vazquez-Yanes & Orozco-Segovia, 1993; Merritt et al.,2007). Where seasonal cues signal a transition to a favourablegermination season, germination might be induced byrelevant environmental factors such as temperature (Merrittet al., 2007). By contrast, for species for which germinationopportunities (e.g. gap formation) limit recruitment to agreater extent than seasonal factors, germination may betriggered by other cues, such as the mechanical and chemicalprocessing that occurs when seeds pass through the gut of ananimal disperser (Traveset, Robertson & Rodríguez-Perez,2007), changes in light regimes caused by gap formation(Finch-Savage & Leubner-Metzger, 2006), or exposure to thesmoke or heat experienced during fire (Flematti et al., 2004,2011). When environments are less predictable (e.g. desert),a more plastic persistence strategy may be favoured suchthat a population’s longevity and germination characteristicsare less rigid (with more variability among individual seeds).This can be thought of as a bet-hedging strategy in which theplant population experiences a trade-off between short-termreproductive success (mean fitness) and long-term risk (fitnessvariance) (Brown & Venable, 1986; Venable, 2007). All ofthese strategies favour the survival of species in their habitat,and thereby enhance the diversity of plant communities.

The duration of persistence has further implicationsfor community composition due to its implications for

inter- and intraspecific competition. Seed persistence maypermit potentially competitive species to coexist by temporalpartitioning of germination, such that species germinateat different times and under different environmentalconditions – a phenomenon known as the ‘storage effect’(Facelli, Chesson & Barnes, 2005). Longer persistence maynot necessarily result in improved competitiveness; loss ofseed vigour over time can lead to slower germination andgrowth, potentially resulting in reduced competitive abilityand persistence in the community (Long et al., 2009). Thus,seed persistence has important consequences for communitycomposition in space and time.

(b) Restoration and conservation management

Seed persistence can inform programs that aim to restoreor rehabilitate degraded lands. For example, topsoil thatis removed prior to mining and returned after operationshave ceased may provide an important source of seedsfor rehabilitation (Bossuyt & Honnay, 2008). While somespecies have long-lived seeds that persist in the topsoil,other species may have transient or short-lived seeds withalternative regeneration strategies. In some cases, seeds arecollected and stored ex situ to be used in the future forrevegetating mined and degraded lands. To optimise thegermination and establishment potential of seeds used forrestoration, it is important to understand the physiologicalchanges, particularly relating to dormancy, that would have



Table 1. Definitions of terms relating to seed persistence

Term Definition

Canopy seed bank Post-maturation seeds retained in the canopy of the parent plant (= serotiny, bradyspory).Conservation seed bank The storage of seeds in controlled ex situ conditions that minimise physical and physiological

changes, for future use by humans (= genebank, storage seed bank).Desiccation-sensitive seeds Seeds that cannot survive drying following maturation. Approximately 8% of flowering plants

bear desiccation-sensitive seeds (= desiccation-intolerant seeds, recalcitrant seeds).Desiccation-tolerant seeds Seeds that can survive drying following maturation. Approximately 92% of the estimated

420000 known species of flowering plants bear desiccation-tolerant seeds (= orthodox seeds).Dormancy cycling Seeds with physiological dormancy can cycle through a gradation of dormancy ‘states’ in

response to their environment, during which the range of conditions in which the seeds areable to germinate widens and contracts.

Ex situ environment Away from the environment into which seeds are naturally dispersed, e.g. in controlled storageconditions in a conservation seed bank, or in a museum jar.

In situ environment The environment into which seeds are naturally dispersed, e.g. the soil of a field or forest.Inherent seed longevity The lifespan of a seed after maturity, as determined by a complex expression of physiological

traits including cellular mobility, internal protective compounds, and the ability of cells toresist and repair damage.

Seed ageing A physiological process in which seeds lose vigour and may eventually die, as detected by the lossof ability to germinate and emerge as a developmentally normal seedling. The process of seedageing is associated with the accumulation of oxidative damage and changes in the ability ofseeds to counteract and repair that damage (Goel et al., 2003; Bailly, 2004; Munne-Bosch et al.,2011). Seed ageing is, to some degree, reversible if antioxidant capacity is recovered (Longet al., 2011a).

Seed decay A process in which the physical integrity of a seed is degraded, ultimately leading to death. Itmay have a physical (e.g. predation or fungal attack) or physiological cause (e.g. cell death thatsubsequently leads to fungal attack).

Seed dormancy A physical or physiological characteristic of a seed that prevents germination whenenvironmental conditions are otherwise suitable for germination (Vleeshouwers et al., 1995).

Seed persistence The survival of seeds from the time they reach maturity on the parent plant until they germinate,are eaten or decayed, or age and die. Seed persistence is influenced by seed characteristics (e.g.dormancy, longevity and defence) and the environment.

Sensitivity cycling Physically dormant seeds can cycle in their sensitivity to environmental conditions that mayovercome dormancy; sensitivity cycling occurs only while the physical barrier to germinationis intact (Jayasuriya et al., 2009).

Soil seed bank The store of seeds that exist in the soil profile, including on the soil surface. Seeds may be ofdifferent species, populations, dormancy states and ages.

occurred in the seeds in situ (Merritt & Dixon, 2011).When managing or recovering rare or threatened species,it is crucial to find out whether there is a persistent seedbank for these species and how to stimulate recruitment orprolong persistence (Fischer & Stocklin, 1997; CALM, 2006).Finally, understanding seed persistence can be importantfor critiquing the validity of vegetation surveys of site andreference communities conducted prior to clearing; above-ground surveys may overlook species (particularly annuals,ephemerals and rare species) that persist in the soil seed bank.

(c) Weed management

An understanding of seed persistence is critical for strategicweed management in natural and agricultural systemsbecause it influences decisions regarding prioritisation ofspecies for control and the duration of management programsnecessary for exhaustion of the weed seed bank (Panetta,2007; Gardarin et al., 2010). Models that predict the durationof weed eradication or containment programmes requireaccurate estimates of seed persistence (Panetta et al., 2011);

however, these data are often absent or limited. Inaccuratepredictions of seed persistence are costly, as underestimatescan lead to re-invasion, and overestimates can lead toresources being wasted on managing a problem that nolonger exists. A further benefit of understanding seedpersistence dynamics is that it can expedite eradicationefforts by inspiring management strategies that encourageseed death via suicidal germination or decay of the weed seedbank (Long et al., 2011b). Thus, knowledge of seed persistencehas both environmental and economic implications in weedmanagement.

(d ) Agricultural management

Beyond the implications for managing weeds, seedpersistence is also an issue for desirable crop and pasturespecies in agriculture. Efficient crop husbandry and harvestdepends on uniform emergence of seedlings in the field,which is influenced by the dormancy and longevity of cropand weed species (Buhler, Hartzler & Forcella, 1997; Forcellaet al., 2000). Crop species are bred to have sufficiently low



Fig. 2. Seed persistence is influenced by the characteristics of seeds or species that confer resistance to exiting the soil seed bank,and by exposure to biotic and abiotic factors in the pre-dispersal and post-dispersal environment.

dormancy so that seeds can germinate when it begins to rain,but not so low as to allow pre-harvest sprouting of seedsdeveloping on parent plants (Gubler, Millar & Jacobsen,2005). Crop and pasture seeds need to persist in ex situ

storage prior to sowing and in the field prior to germinating(Nagel & Borner, 2010). Typically crop seeds only persistin soils for a short period between planting and rainfall,but in crop–pasture rotation systems, it is advantageousthat seeds of pasture species are dormant and can persistfor 2–3 years (e.g. hard-seeded clover) so that they escapeherbicide treatments during the cropping component ofthe cycle (Nichols et al., 2007). For some crop species, e.g.oilseed rape, environmental stress can cause seeds to re-enterdormancy and persist until a later season, when they mayemerge as weeds in a subsequent crop (Pekrun, Lutman &Baeumer, 1997). Just how long seeds persist in agriculturalsystems depends on many of the same biotic and abioticfactors that affect seeds in natural systems, but the effectsof disturbance (e.g. from tillage) and predation (e.g. bybirds and ants) may be more pronounced in agriculturalsystems.

II. SEED CHARACTERISTICS THAT INFLUENCEPERSISTENCE

Here we outline the physical and physiological characteristicsof seeds that influence their ‘resistance’ to exiting the soilseed bank through germination, ageing, predation and decay.Seed characteristics can vary according to the species andseed population, and are altered by ‘exposure’ to abioticand biotic factors in pre- and post-dispersal environments todetermine how long seeds persist in soils. Nevertheless, thereappears to be an inherent genetic basis to persistence thatconsistently results in some species or populations survivinglonger than others in different environments. For example,the persistence of seeds in the field or in uncontrolled storageconditions tends to correlate positively with their longevityin controlled ageing tests or controlled storage conditions(Bekker et al., 2003; Long et al., 2008; Nagel & Borner,2010), and up to half of the variability in the data can beattributed to a genetic basis (Bekker et al., 2003). Walterset al. (2005c) observed consistent rankings for the ex situ seedlongevity of species tested in separate experiments, againsuggesting a genetic component, but in this study there



was no correlation between in situ persistence and ex situlongevity. The inference from these studies that a geneticbasis underpins seed longevity and, in some cases, persistence,motivates us to understand those characteristics of seedsthat confer resistance to germination, ageing, predation anddecay.

(1) Seed dormancy and germination

The propensity of seeds to exit the soil seed bank bygerminating is influenced by seed dormancy (see definitionin Table 1). Based on the dormancy classification of Baskin &Baskin (2004), which is reviewed comprehensively in Finch-Savage & Leubner-Metzger (2006), seed dormancy can bebroadly divided into (i) physical, in which seeds possess animpermeable coat that prevents water reaching the embryo;(ii) physiological, in which the balance of endogenoushormones prevents germination; (iii) morphological, in whichthe embryo is not fully developed at the time of seeddispersal and requires time to grow; (iv) morphophysiological,in which the embryo is undeveloped and a hormoneimbalance inhibits further development and germination;and (v) combinational, in which seeds possess a physicalbarrier to water uptake as well as physiological dormancy.Reviews of the mechanisms underlying the most commonlyoccurring dormancy types are available: physical dormancy(Baskin, 2003) and physiological dormancy (Finch-Savage &Leubner-Metzger, 2006; Finkelstein et al., 2008).

Some authors have deemed that physiological seeddormancy is neither required for, nor contributes to,persistence (Thompson et al., 2003; Honda, 2008; Thompson& Ooi, 2010). This view is based on the concept of separatedormancy loss and stimulation of germination (Thompsonet al., 2003; Thompson & Ooi, 2010) so that seeds canpersist in a non-dormant state while awaiting stimulation ofgermination. From this perspective, light, smoke, nitrate ordiurnal temperature alternations do not break dormancy,but stimulate germination. However, although this view iscompelling, it is not supported by current literature on theregulation of dormancy and germination, which convey theconcept of a dormancy continuum (Finch-Savage & Footitt,2012). In this case, Finch-Savage & Leubner-Metzger (2006)argue that dormancy has a number of layers, such thatremoval of the final layer of dormancy (e.g. exposure tolight) is synonymous with the stimulation or induction ofgermination. Thus a wide range of environmental signalscan alter dormancy, but seeds must be exposed to themin sequence for dormancy to be fully removed and forgermination to proceed. Dormancy loss and stimulationof germination are therefore not separate events (Finch-Savage & Footitt, 2012). Following this widely acceptedview, dormancy can be considered to benefit persistence,even if it is not strictly required. This is because dormantseeds typically take longer to germinate than non-dormantseeds (Honda, 2008; Saatkamp et al., 2011b) and may bemore resistant to ageing, thus they can persist longer in thesoil seed bank.

In the case of physically dormant seeds, the impermeableseed coat favours persistence, as the seed can only exit theseed bank by germinating once the seed coat is disruptedand water can reach the embryo (Baskin, 2003). Moreover,an intact impermeable seed coat protects an embryo fromfluctuations in humidity that could accelerate ageing, andthus may also preserve the inherent longevity of physicallydormant seeds (Long et al., 2008). Similarly, seeds with deeperphysiological dormancy may have a longevity or persistenceadvantage over seeds that are less dormant. In Turner et al.(2009), after-ripening at higher water contents led to a steadyrise in total germination of seeds of species that differedin their initial depth of dormancy, but then viability beganto decline in the less-dormant species. Reactive oxygenspecies (ROS), which are highly reactive atoms, molecules orradicals that accumulate during normal metabolism, stress(Foyer & Noctor, 2005), and ageing (Bailly, 2004), may be lessharmful in seeds with deeper physiological dormancy due totheir interaction with antioxidants and hormones associatedwith dormancy (Bailly, 2004; Bahin et al., 2011); however,this hypothesis is yet to be tested and the mechanism yetto be shown. Nevertheless, the assertion of Thompson et al.(2003) that dormancy does not contribute to persistence is,in light of these lines of evidence, a premature dismissalof an important relationship; their use of categorical datainferred from separate studies of persistence and dormancyfor different seed populations may have led to an erroneousconclusion. The contribution of dormancy to persistenceremains an issue in need of further targeted physiologicaland ecological studies.

(a) Conditions that alleviate dormancy

The environmental conditions that alleviate seed dormancy,and thus influence whether seeds leave the soil seed bankvia germination, depend on the type of dormancy. Forphysically dormant seeds with a water-impermeable seed orfruit coat, seeds can be rendered permeable, and thereforenon-dormant, by scarification, wet heat and dry heat in thesoil seed bank (Baskin & Baskin, 2001; Traveset & Verdugo,2002; van Klinken, Flack & Pettit, 2006). Physiologicaldormancy is alleviated by hormonal changes within theseed that are driven by changes in the seed’s physical (e.g.moisture, temperature, light) and chemical (see examplesbelow) environment. The roles of moisture and temperaturein alleviating physiological dormancy are particularly wellstudied, and the following naturally occurring processes maycontribute to dormancy loss: (i) dry after-ripening (sustaineddry conditions) (Foley, 1994; Chauhan & Johnson, 2008;Iglesias-Fernandez, del Carmen Rodríguez-Gacio & Matilla,2011); (ii) cold and warm stratification (wet conditionsbelow or above 10◦C, respectively) (Schutz & Rave, 1999;Turner et al., 2006; Footitt et al., 2011, 2013); (iii) wet-drycycling (alternating periods of wetting and drying) (Gallagher,Steadman & Crawford, 2004; Batlla & Benech-Arnold, 2006;Hoyle et al., 2008a; Long et al., 2011b); and (iv) alternatingtemperatures (Batlla & Benech-Arnold, 2006; Footitt et al.,2011; Long et al., 2011c).



Light influences dormancy loss in imbibed seeds (Goggin,Steadman & Powles, 2008; Goggin et al., 2011), with somegrass species losing dormancy when stratified in darkness,but not in light (Steadman, Bignell & Michael, 2004a; Longet al., 2011c). Light can also remove dormancy through asignal transduction pathway involving the photoreceptorphytochrome and the plant growth hormone gibberellin.Phytochrome action degrades a repressor of gibberellinsynthesis in Arabidopsis thaliana seeds (Oh et al., 2006) and alsoincreases Datura ferox seed sensitivity to gibberellins (Arana,Miguel & Sanchez, 2006), both of which relieve dormancyresulting in the completion of germination. See also Finch-Savage & Leubner-Metzger (2006) for a discussion of therole of light in dormancy alleviation and germination.

Physiological dormancy may also be alleviated, or by-passed, via the action of naturally occurring exogenouscompounds in the environment including: (i) karrikins(Flematti et al., 2004; Long et al., 2011c) and glyceronitrile(Flematti et al., 2011) from smoke and ash; (ii) nitrates(Chauhan, Gill & Preston, 2006; Finch-Savage et al., 2007;Footitt et al., 2013) from decomposing biological materialsand synthetic fertilisers; (iii) nitric oxide, derived from thein vivo conversion of organic and inorganic nitrates (Bethke,Libourel & Jones, 2007; Sirova et al., 2011); and (iv) ethylene(Matilla & Matilla-Vazquez, 2008; Lin, Zhong & Grierson,2009).

Physiologically dormant seeds can vary in their sensitivityto these physical and chemical signals according to thespecies, population, seed age and season (Baker et al., 2005;Long et al., 2011b,c). Although the conditions that alleviatedormancy in crop and wild species are relatively wellunderstood, further research is needed to understand thehow dormancy is re-induced; for example, dormancy re-induction could involve threshold limits on the amount oftime that seeds spend imbibed at a particular temperature orenduring stressful conditions. Together, alleviation and re-induction of physiological dormancy constitute an importantecological process known as dormancy cycling.

(b) Dormancy cycling

Physiologically dormant seeds act as environmental sensorsthat can adjust their depth of dormancy in response to arange of signals (Finch-Savage & Leubner-Metzger, 2006).For example, in temperate soils, some signals (e.g. soiltemperature and moisture) occur as slow seasonal changesthat indicate a suitable time of year and climate forgermination and seedling establishment (i.e. a temporalwindow) (Vleeshouwers, Bouwmeester & Karssen, 1995;Benech-Arnold et al., 2000; Vleeshouwers & Bouwmeester,2001; Footitt et al., 2011, 2013). These signals are integratedover time to alter the depth of dormancy, and consequentlythe sensitivity of the seed to a second set of signals thatremove the final layers of dormancy to allow the completionof germination (e.g. by light, smoke, nitrate, alternatingtemperatures; Long et al., 2011b,c; Footitt et al., 2013). Thus,this second set of signals indicate in a more immediateway that conditions are suitable to terminate dormancy and

induce the completion of germination (i.e. a spatial window ofappropriate soil depth, temperature and moisture, and lackof competing plants, possibly following fire). If the correctspatial window (i.e. favourable habitat conditions) does notoccur then the temporal window will close for another year.In this way, the dormancy state of seeds aligns with theseasons, thereby determining the optimum time for plantestablishment, and enabling the spreading of a population’sgermination events through time (Batlla & Benech-Arnold,2010).

By its nature, dormancy cycling is probably not astrategy specifically to enhance seed persistence in thesoil, but to ensure that germination occurs in conditionsthat are favourable for subsequent competition andreproduction. Nevertheless, seeds undergoing dormancycycling persist longer than they would if dormancy losswas a unidirectional process that rendered them non-dormant and germinable throughout the seasons; indeed,physiologically dormant seeds can persist for more thana decade in both dry (Gutterman, 2000a) and moist(Hill & Kloet, 2005) soil conditions. Dormancy cyclingmay follow a regular or irregular pattern depending onthe climate and habitat (Gutterman, 2000a; Long et al.,2011b). Further, physiologically dormant seeds may maintaininherent rhythms of dormancy that continue irrespective oftheir environment (Froud-Williams, Hilton & Dixon, 1986;Gutterman & Gendler, 2005). Changes in dormancy stateunder natural conditions can be linked to the molecularmechanisms of dormancy identified in the laboratory. Forexample, in Arabidopsis thaliana, abscisic acid (ABA) signallingwas associated with deeper dormancy in winter, whereasalleviation of dormancy in spring coincided with repression ofABA signalling and enhanced gibberellic acid (GA) signalling(Footitt et al., 2011). See Finch-Savage & Leubner-Metzger(2006) and Finkelstein et al. (2008) for more comprehensivediscussions of the roles of these hormones maintaining andalleviating dormancy.

Physically dormant seeds do not undergo dormancycycling, as once they are rendered non-dormant they cannotre-enter physical dormancy because the change in seedcoat permeability cannot be reversed (Jayasuriya, Baskin& Baskin, 2009). However, so long as the physical barrierremains intact, physically dormant seeds can cycle in theirsensitivity to factors that eventually overcome dormancy,such as high temperatures (Jayasuriya et al., 2009). Thisprocess is known as ‘sensitivity cycling’, and is distinct from‘dormancy cycling’, which involves loss and re-induction ofdormancy in physiologically dormant seeds (Jayasuriya et al.,2009).

(c) Germination conditions

Seeds germinate when environmental conditions (moisture,oxygen, temperature and light) indicate a temporal or spatialwindow for emergence and survival. Dormancy can preventseeds from germinating under favourable conditions, buteven low-dormancy and non-dormant seeds can persist insoils if environmental conditions do not support germination



(Ooi, Auld & Whelan, 2007). [For comprehensive reviews ofthe molecular and physiological aspects of seed germination,see Holdsworth, Bentsink & Soppe (2008), Nonogaki, Bassel& Bewley (2010) and Rajjou et al. (2012)]. Moisture isneeded for embryos to imbibe and germinate, and differentspecies have different threshold water potentials that cansupport germination at different temperatures (Rowse &Finch-Savage, 2003). This is relevant under saline conditions(Zhang et al., 2010), and also in environments where moistureis not available year round (Gutterman, 1994, 2000a).Although seeds of many species require atmospheric oxygenconcentrations (oxygen constitutes approximately 21% ofthe air) to germinate, others, particularly those from aquaticenvironments, can germinate in low-oxygen and anaerobicconditions (Fenner & Thompson, 2005); see also Section V.

(2) Inherent seed longevity

A key determinant of seed persistence is inherent seedlongevity (Long et al., 2008), which is a complex expressionof physiological traits including cellular mobility, internalprotective compounds, and the ability of cells to resistand repair damage. The two main factors that influencebiochemical ‘ageing’ reactions in seeds are seed wateractivity and temperature (Ellis & Roberts, 1981; Walters,Hill & Wheeler, 2005a). Seed water activity is influencedby the humidity (or water potential) and temperature ofa seed’s environment and by seed lipid content (Walters,1998). Seed water activity and temperature influence theviscosity of the cytosol, membrane fluidity and integrity,the activity of antioxidants, and rates of transcriptionand translation (Walters et al., 2005a). Consequently, testsfor assessing inherent longevity involve placing seeds incontrolled temperature and humidity conditions to test theirphysiological ‘resistance’ to the loss of germinability andviability associated with ageing (Lehner et al., 2008; Longet al., 2008; Probert et al., 2009). The literature on ex situlongevity testing conditions includes various names (e.g.accelerated ageing, controlled deterioration and controlledageing) and methods of execution, but their use hascontributed significantly to understanding the characteristicsoutlined below that underpin seed longevity.

(a) Desiccation tolerance

Most species studied to date have desiccation-tolerant seedsthat are shed with low water content following maturationdrying. Seeds can survive desiccation partly due to theaccumulation of non-reducing sugars and induction of lateembryogenesis abundant (LEA) proteins during the latestages of seed development. These components facilitateintracellular ‘glass formation’ when cells lose water, whichreduces molecular mobility and restricts chemical reactions(Colville & Kranner, 2010; Leprince & Buitink, 2010). Seedscan remain in this so-called ‘glassy state’ of low metabolicactivity for long periods (Shen-Miller et al., 1995; Sallon et al.,2008), and thus persist in dry conditions in situ and ex situ.

Desiccation-sensitive seeds are most common in speciesnative to tropical wet climates, and are often containedwithin fleshy fruit, but can occur in species from a range ofenvironments and life forms (e.g. the temperate tree speciesQuercus robur) (Finch-Savage, 1992; Berjak & Pammenter,2008). Desiccation-sensitive seeds are shed in an hydratedand metabolically active state, and usually germinate rapidly,forming seedling banks. These seeds perish if they drybelow a critical water content, but some desiccation-sensitiveseeds can survive for several months in moist conditions(Le Tam et al., 2004), due to dormancy (Greggains et al.,2000; Jayasuriya et al., 2010) or delayed germination (Pina-Rodrigues & Figliolia, 2005). For example, seeds of Podocarpusangustifolius form a persistent soil seed bank (Ferrandis, Bonilla& Osorio, 2011), which is highly unusual, but indicates thatdesiccation tolerance is not a strict prerequisite for seedpersistence.

(b) Sugars

Seed sugars such as sucrose, raffinose, stachyose andverbascose can help to protect proteins and phospholipidsfrom heat- and desiccation-induced damage, and thusinfluence seed longevity (Bernal-Lugo & Leopold, 1995,1998). Sucrose by itself can protect phospholipid membranesin in vitro models and thus has been implicated in conferringdesiccation tolerance and seed longevity (Caffrey, Fonseca& Leopold, 1988), but no such positive correlation wasfound in maize seeds (Bernal-Lugo & Leopold, 1995).However, many studies suggest that oligosaccharides suchas raffinose are important mediators of glassy-state stabilityand membrane fluidity due to their interaction with sucrose(Caffrey et al., 1988; Leopold, Sun & Bernal-Lugo, 1994;Walters, 1998; Walters et al., 2001); indeed, the ratioof sucrosyl-oligosaccharides to sucrose is a reasonableindicator of storage stability (Steadman, Pritchard & Dey,1996). It should be noted that these studies all rely oncorrelative evidence and an empirical study found no directlink between oligosaccharide content and increased seedlongevity (Buitink, Hemminga & Hoekstra, 2000). Thecontribution of sugars to seed longevity and persistencethus remains contentious.

(c) Seed lipids and membrane integrity

The lipid composition of cellular membranes can influenceseed longevity, and the membranes of longer-lived seeds tendto be more stable (Golovina, Van As & Hoekstra, 2010). Seedoil content may not directly affect longevity (Probert et al.,2009; Walters et al., 2005c; but see Nagel & Borner, 2010) orpersistence (Gardarin et al., 2010), but lifespan does correlatewith the degree of saturation of membrane lipids (Hoekstra,2005). Seed ageing causes changes in the organisation oflipid reserves and their thermal properties (Walters et al.,2005b), loss of membrane phospholipids (in Arabidopsis thalianaseeds, this may be due to phospholipase D activity; Devaiahet al., 2007), and lipid peroxidation resulting from ROSattack on the double bonds of unsaturated fatty acids



(Priestly & Leopold, 1979; Murthy & Sun, 2000). Decreasedfatty acid unsaturation, accumulation of lipid degradationproducts such as malondialdehyde, and increased electrolyteleakage due to membrane damage are all indicators of lipidperoxidation (Corbineau et al., 2002; Mira et al., 2011). Theinvolvement of membrane integrity and lipid composition inseed persistence in the soil has not been explored and it islikely that fluctuating field conditions would greatly influencelipid metabolism, peroxidation and membrane stability.

(d ) Proteins

The damage that accumulates within seeds duringmaturation drying and after dispersal must be repairedupon rehydration so that healthy seedlings can emerge.Many proteins associated with repair and protection againstoxidative stress are induced during the early stages ofimbibition and are important determinants of seed longevityand vigour. For example, DNA ligases are induced duringimbibition of Arabidopsis thaliana seeds to repair DNAstrand breaks (Waterworth et al., 2010) and L-isoaspartylO-methyltransferase repairs age-related protein damage(Oge et al., 2008). Dehydrins are LEA proteins that areinvolved in desiccation tolerance, and reduced expressionof LEA14 in Arabidopsis thaliana seeds decreased theirlongevity (Hundertmark et al., 2011). Heat shock factors(HSF) may also affect seed longevity, since expression levelsof the seed-specific HSFA9 correlated positively with seedlongevity in studies of transgenic sunflower (Almogueraet al., 2009) and tobacco (Tejedor-Cano et al., 2010). Certainseed proteins, rather than actively repairing damage, canact as buffers against degradation of more importantseed macromolecules: seed storage proteins and molecularchaperones are preferentially carbonylated (oxidised) (Jobet al., 2005; Rajjou et al., 2008), thus protecting otherproteins and cellular components from oxidative damage(Rajjou & Debeaujon, 2008) (see below for a detaileddiscussion on oxidative damage and antioxidant defencein seeds). Although some of the proteins associated with seedlongevity in vitro have been described (Rajjou et al., 2008),there are undoubtedly many more that contribute to seedpersistence in the soil, where exposure to soil and climateconditions could induce up- and downregulation of a range ofproteins.

(e) Key antioxidants: capacity to resist deterioration

There are many comprehensive reviews on the role of ROSas agents of both damage and signalling in plant tissues andseeds, e.g. Bailly (2004), Foyer & Noctor (2005), Bailly, El-Maarouf-Bouteau & Corbineau (2008), and Kranner et al.(2010). In the context of seed longevity and persistence,loss of seed viability during the ageing process is associatedwith the accumulation of oxidative damage and changes inthe ability of seeds to counteract and repair that damage(Goel, Goel & Sheoran, 2003; Bailly, 2004; Munne-Boschet al., 2011). As seeds age, their loss of viability is mainlydue to ROS-mediated damage to cellular membranes.

Non-enzymatic antioxidants such as glutathione (a sulphur-containing tripeptide) and tocochromanols (lipid-solublemolecules belonging to the Vitamin E family) form thebasis for ROS-scavenging in dry seeds, and the redox stateof glutathione is a marker of seed viability (Kranner et al.,2006; Seal et al., 2010; Birtic et al., 2011). The involvementof antioxidants in seed longevity has been demonstratedin several studies using mutant plants with altered levelsof antioxidant molecules or enzymes. For example, seedlongevity in Arabidopsis thaliana was shortened by combineddeficiencies of glutathione and ascorbic acid or ascorbic acidand catalase (Clerkx et al., 2004a), or by tocochromanoldeficiency (Sattler et al., 2004; Mene-Saffrane, Jones &DellaPenna, 2010). Maize seeds deficient in phytic acid,which may help to protect against oxidative stress, were alsomore vulnerable to accelerated ageing (Doria et al., 2009).By contrast, over-expression of superoxide dismutase andcatalase in tobacco resulted in enhanced seed longevity (Leeet al., 2010). In the soil, seeds undergo cycles of dehydrationand rehydration which can extend seed persistence byreinstating antioxidant capacity (Long et al., 2011a) throughthe induction of antioxidant enzymes (e.g. catalase andsuperoxide dismutase) and the reduction of glutathionedisulphide via increased glutathione reductase activity. Thus,the inherent antioxidant content of seeds at maturity, andtheir ability to recover antioxidant capacity rapidly uponimbibition, contributes to their longevity and persistence.

(f ) Resistance to genetic degradation

Seeds have the ability to repair DNA, which can be degradedprogressively during desiccation and storage. Unlike DNAreplication, DNA repair is activated within minutes ofimbibition (Nonogaki et al., 2010). When DNA repair isblocked, survival of embryos with previously degradedDNA is reduced (Osborne & Boubriak, 2002). Relativelyshort imbibition treatments such as priming can reducechromosomal aberrations and increase the number ofhealthy seedlings, and this is thought to result from repairmechanisms (Waterworth et al., 2011). These mechanismscould also be activated during cycles of dehydration andrehydration while the seeds persist in soils. Indeed, thesurvival of seeds in the dormant state may be due in partto their ability to maintain active DNA repair, even thoughreplicative DNA synthesis is blocked (Osborne & Boubriak,2002). The activity of DNA repair enzymes in dormant seedscan be as efficient as that in germinating seeds (Villiers,1974). Although DNA repair enzymes are not stable and loseactivity during storage, resulting in progressively delayedrepair and thus delayed germination, these enzymes may beregenerated during cycles of dehydration and rehydration(Boubriak et al., 1997). If the seeds are dormant, such repairmechanisms could become active before seeds progresstowards germination and otherwise abnormal seedlingdevelopment. For a more detailed review of DNA repairmechanisms, see Rajjou et al. (2012) and Waterworth et al.

(2011).



(3) Seed characteristics related to dispersal,defence and germination

Beyond its capacity to resist germination and ageing, a seed’spropensity to remain alive in the soil seed bank also dependson its dispersal environment and ability to resist predationby animals and decay by microorganisms. These factors areinfluenced by seed size and the specific characteristics of seedcoats, appendages and exudates.

(a) Seed size and embryo-endosperm proportions

Morphological characteristics of seeds that influencepersistence include their size and the relative proportionsof embryo and endosperm. In terms of predation risk, largeseed size can mean that seeds are easier for predators tofind, but it can also reduce predation in some circumstances(Blate, Peart & Leighton, 1998; Rodriguez-Perez & Traveset,2007; but see Dechaine, Burger & Burke, 2010; Bradford& Westcott, 2011; Tasker et al., 2011). This may be becausepredators are satisfied by eating fewer seeds, because ofthe increased handling costs associated with larger, andoften harder, seeds, or because the large ‘reward’ offered bylarger seeds is more efficiently handled by caching for laterconsumption (Yang, Yi & Niu, 2012).

Numerous studies have explored correlations of seedsize and shape with persistence (Bekker et al., 1998a, 2003;Hodkinson et al., 1998; Thompson et al., 1998, 2001; Funeset al., 1999; Moles, Warton & Westoby, 2003; Honda, 2008;Zhao, Wu & Cheng, 2011b); see also Section III.2c. Bekkeret al. (1998a) found that larger seeds and seeds with largesurface area to volume ratios tend to be shorter-lived andare not incorporated into the soil as easily as their smaller,rounder counterparts, which fall easily through cracks andare more readily transported by earthworms. A positiverelationship between small seed size and longer persistencewas also demonstrated in the flora of Britain (Hodkinson et al.,1998), Argentina (Funes et al., 1999), Iran (Thompson et al.,2001) and northern China (Zhao et al., 2011b). Moreover,small rounded seeds may be more resistant to fire, andthereby more persistent in environments where fire frequencyis high (Gomez-Gonzalez et al., 2011). However, other studieshave reported that larger seeds persist longer (Moles et al.,2003; Holzel & Otte, 2004), or that persistence is notcorrelated with size (Leishman & Westoby, 1998, in a studyof 101 Australian species). There was no link between seedsize and longevity in a controlled ageing study of 195 species,but endospermic seeds tended to be shorter-lived thannon-endospermic seeds (Probert et al., 2009). Contradictoryresults do not necessarily discount the contribution of seedsize and anatomical features to persistence, as the influenceof climate, soil and other site characteristics (such as thepresence of predators) in situ may determine whether theircontribution is significant.

(b) Seed nutritive value for predators

Once a seed is detected by a predator, its nutritionalcontent will be important in determining if it is eaten.

Seeds containing more oil and energy and with less fibreare typically preferred by predators and therefore tend to beless persistent (Dechaine et al., 2010), but they may be morelikely to be cached than eaten immediately in some cases(Xiao et al., 2008; Yang et al., 2012). Similarly, the secondarymetabolite composition of the seed (or its surrounding tissues)can influence the physiological or metabolic cost of seedprocessing (Cipollini & Levey, 1997; Vander Wall, 2010),the risk of gut and kidney damage incurred by consumingthe seed (Chung-MacCoubrey, Hagerman & Kirkpatrick,1997), and thus the probability of immediate predation orcaching, and therefore of seed survival.

(c) Characteristics of seed coats and other surrounding tissues

The tissues surrounding the embryo and endosperm (ifpresent), including the seed coat, mucilage and any othercomponents of the dispersal unit (e.g. a woody endocarp orindehiscent fruit) offer both physical and chemical protectionagainst predation and microbial decay, as reviewed inFuerst et al. (2011) and Dalling et al. (2011). At the simplestlevel, the colour of seeds can affect their susceptibility topredation (Lev-Yadun & Ne’eman, 2013), and can be anindicator of the content of antimicrobial compounds inthe seed coat (Lepiniec et al., 2006). In many physicallydormant species, a densely packed layer of palisade cellswith water-repellent properties shields the embryo from theenvironmental fluctuations in moisture that can influencelongevity (Baskin & Baskin, 2006). Hard-seeded species, suchas Nelumbo and Cassia spp., have persisted in the soil for up to1300 years, apparently protected from microorganisms andimbibition by their hard coat (Smith & Berjak, 1995; Baskin& Baskin, 2001). Even in species that do not exhibit physicaldormancy, thicker seed coats have been associated withgreater persistence, probably due to their greater resistanceto predation and decay (Gardarin et al., 2010). Indeed, traitssuch as seed ‘toughness’ (Blate et al., 1998; Lundgren &Rosentrater, 2007), and the presence of mucilage whichglues the seed to the substrate (Engelbrecht & Garcia-Fayos, 2012) all make seeds more difficult for predatorsto process and therefore less attractive. In some species, awoody endocarp (e.g. Chrysanthemoides monilifera; Schoemanet al., 2010) or indehiscent seed pod or silique (e.g. Raphanusraphanistrum; Cousens, Young & Tadayyon, 2010) may inhibitgermination by limiting expansion of the seed within, despitesuch tissues often being permeable to water and light (Longet al., 2011b).

In terms of chemical protection, phenolic compounds,which are mainly localised in the testa (reviewedin Debeaujon, Leon-Kloosterziel & Koornneef, 2000),contribute to seed longevity and persistence by limiting thewater and oxygen permeability of seed coats and by acting asantioxidants, antimicrobial and anti-predation compounds(Hendry et al., 1994; Lepiniec et al., 2006; Pourcel et al.,2007; Davis et al., 2008; Xiao, Chang & Zhang, 2008).For example, seed ortho-dihydroxyphenol concentrationscorrelated positively with in situ persistence in a study on 81species (Hendry et al., 1994), indicating that its antimicrobial



properties confer a persistence benefit. Thus, the chemicalcomposition of the seed coat can play a crucial rolein determining the susceptibility of seeds to ageing andmicrobial degradation.

(d ) Seed appendages

Structures attached directly to seeds [e.g. arils andelaiosomes (oil bodies)], or surrounding fruit tissues (e.g.awns, wings and fleshy fruit) can facilitate seed dispersaland influence persistence in natural and agriculturalenvironments (Benvenuti, 2007a,b). Movement of seeds tobelow the soil surface can protect them from predatorsand provide a less fluctuating environment for germination.The 4.5% of angiosperm species that possess seeds withelaiosomes are adapted to being dispersed underground byants (Lengyel et al., 2010), whilst awned seeds (common inthe Poaceae) can drill themselves underground as their awnsunwind and rewind during wetting and drying (but seePeart, 1984). By contrast, seeds that are surrounded by fleshytissues are often dispersed after being consumed by birdsand mammals (e.g. Traveset & Verdugo, 2002; Dennis et al.,2007; Vivian-Smith & Gosper, 2010). Gut passage throughanimals can scarify seeds and deposit them with naturalfertiliser, thus promoting their ready germination, but alsopotentially leaving them exposed to secondary predation(Bradford & Westcott, 2011; see Section V.3f ).

(e) Seed exudates

Imbibing and germinating seeds can exude compoundsthat influence other seeds and the growth of microbesin their immediate environment, thereby influencingseed persistence. Exuded chemicals such as lepidimoide(Hasegawa et al., 1992) and ethylene (Linkies & Leubner-Metzger, 2012) can trigger neighbouring seeds to germinate,potentially promoting them to leave the soil seed bank,whilst vanillic acid (Kushima et al., 1998) and sundiversifolide(Ohno et al., 2001) are allelopathic exudates that inhibit thegermination of nearby seeds, encouraging their persistence.Seed persistence in soil is also threatened by pathogenicmicrobes, whose growth can be encouraged by seed exudatesof reduced carbon compounds (Roberts et al., 2009), ordiscouraged by proteinaceous inhibitors of microbial activity(Rose et al., 2006) such as peroxidases (Fuerst et al., 2011).Both the quantity and composition of the exuded compoundscan influence persistence by signifying the seed’s presence tohost-specific pathogens and neighbours (Roberts et al., 2009;Elzein et al., 2010). Further research into seed exudatesshould address whether these chemicals occur widely amongspecies, or whether exudates are generally species-specific,thus exploring whether they are the general cues that enableseeds to sense each other (Tielborger & Prasse, 2009).

(f ) Symbioses with endophytic microorganisms

Both fungi and bacteria can exist in endophytic symbioseswith seeds and impact their persistence; these internally

penetrating, intergenerational associations are distinct fromassociations that form when microorganisms present in theenvironment colonise seeds during imbibition or germination(see Section V.2d for a discussion of the impacts of soil-bornepathogenic microorganisms on seed persistence). Differentmicroorganisms can associate specifically with particularplant species and genotypes (Nelson, 2004; Liu et al., 2012),and the nature of their relationship may be neutral at theseed stage (e.g. bacterial Pseudomonas spp. present in seeds thatlater affect seedling vigour of the cactus Pachycereus pringlei;Puente, Li & Bashan, 2009) or ‘beneficial’ (e.g. mycchorizalfungi promoting germination of orchid seeds; Batty et al.,2001); pathogenic organisms are typically excluded from thedefinition of endophytes (Schulz & Boyle, 2005).

Fungal endophytes infect plants and seeds of a wide rangeof species and environments (Schulz & Boyle, 2005), but areparticularly well documented in temperate grasses. Amongthe most-studied fungal endophytes are the seed-transmittedspecies of the fungal genera Epichloe, Neotyphoditum,and Acremonium, and their mutualistic interactions witheconomically important pasture grasses (Richardson, 1996;Schardl, Leuchtmann & Spiering, 2004). The hyphae of thesefungal endophytes infect seeds during seed development(Schardl et al., 2004), and the relationship can influence seedcharacteristics directly or indirectly. For example, in a studyof the effects of the fungal endophyte Acremonium loliae onthe seed biology of two grasses, Lolium perenne and Festucaarundinacea, infected plants of Festuca arundinacea producedmore than twice as many filled seeds as uninfected plants(Clay, 1987). This greater seed production may be attributedto the mutualistic benefits conferred by the fungus in theparental environment (see Section IV), as fungal endophytescan confer vigour and drought-tolerance benefits to infectedplants (Clay & Holah, 1999), enabling them to producemore seeds. More seeds from infected plants of both grassesgerminated within 8 days of sowing than did seeds fromuninfected plants (Clay, 1987), ultimately indicating thatseeds from infected plants may be less persistent in thesoil than seeds from uninfected plants. There are far fewerreports of studies into endophytic bacterial relationships thanfungal relationships with seeds, and the effects of endophyticbacteria on seed persistence – particularly involving naturalcolonisation – needs further investigation.

III. SPECIES CHARACTERISTICS RELATED TOSEED PERSISTENCE

Given that there is likely a genetic basis to seed persistence(see Section II), we can expect to see patterns in persistenceacross species. Critical genes or alleles of key genes that confera persistence benefit may be shared among related species,among species with similar reproductive traits and amongthose from the same native range that have presumablybeen exposed to similar selection pressures. Here we discussseveral characteristics of species that may correlate with



seed persistence, and thus may be used to inform predictivemodels.

(1) Phylogeny

Seed persistence can be associated with taxonomic groups,due to the tendency for related species to exhibit similarlongevity, dormancy, and probably also defence traits.Some orders and families are inherently short-lived (Liliales,Apiaceae, Campanulaceae, Ericaceae, Melianthaceae) orlong-lived (Caryophyllales, Juncales, Myrtales, Malvaceae,Myrtaceae), while others contain species with wide-ranginglongevities (Fagales, Lamiales, Asteraceae, Brassicaceae,Fabaceae, Gentianaceae, Poaceae, Primulaceae, Solanaceae;Hodkinson et al., 1998; Walters et al., 2005c; Probert et al.,2009). Similarly, dormancy types tend to be consistent withingenera and families (Baskin & Baskin, 2001). The trends caneven exist at the population level, with quantitative traitloci (QTL) that correspond to seed longevity and dormancyhaving been identified for different ecotypes of Arabidopsisthaliana (Clerkx et al., 2004b; Bentsink et al., 2010). Defencetraits may also present as a pattern among related species,given that seed and fruit morphologies which may favouror inhibit attack are often common within a family (Janzen,1971). Thus, although phylogeny itself may not be a causativepredictor of seed persistence, the co-occurrence of particularpersistence-related genes among related species means thatphylogeny could be a strong correlate of persistence, andshould be investigated further.

(2) Life history and reproduction

The capacity to form a persistent seed bank can be correlatedwith the life history of a species, but there is little evidencethat reproductive syndrome (self- or cross-pollination) orfecundity correlate with seed persistence.

(a) Life history

Annual and biennial species had smaller and more persistentseeds than perennials in grassland and arable systems ofnorthwest Europe (Thompson et al., 1998; Honda, 2008), atalpine sites in South America (Kalin Arroyo et al., 1999)and North America (Chambers, 1995). However, seedpersistence was not correlated with life history in calcareousgrasslands of the Swiss mountains (Stocklin & Fischer, 1999).Therefore, life history is not always a reliable predictor ofseed persistence.

In systems exhibiting an initial floristic model, whereby allspecies recruit immediately following disturbance, differencesin seed persistence may exist between short-lived species thatare only present in the initial community, and long-livedspecies that make up the climax community. For instance, inarid Australia, short-lived ephemeral species that recruit afterfire have a persistent seed bank to ensure their survival untilthe next fire, whereas perennial grasses and shrubs of theclimax community do not appear to have a persistent seedbank (Wright & Clarke, 2009), instead relying on serotiny,

annual seed rain or the ability to re-sprout (Wright, 2008). Inaddition, tropical rainforests consist of pioneer tree species,which germinate in light-filled canopy gaps, and non-pioneer(climax) tree species, which are able to germinate in the low-light conditions beneath the canopy (Baskin & Baskin, 1998),and there is evidence that climax species are less likely to formpersistent seed banks than pioneer species (Baskin & Baskin1998, Oke, Oladipo & Isichei, 2006; Dalling & Brown, 2009).

(b) Reproductive syndrome

Seed production via self-pollination, out-crossing or apomixishas no apparent influence on seed longevity, as demonstratedby congeneric species of Ipomoea (Astegiano, Funes &Galetto, 2010) and Wahlenbergia (Kochanek et al., 2009),which exhibit different pollination syndromes but similar seedlongevities. However, a greater degree of self-compatibilityhas been associated with shallower physiological dormancyin sunflower (Gandhi et al., 2005). Beyond pollinationsyndromes, it would be interesting to compare the seedlongevity of species that reproduce both sexually andasexually, such as the invasive succulents Bryophyllum spp.,with that of species that reproduce only via seeds, to learnwhether seeds offer the former a dispersal benefit in time (i.e.a persistence benefit) as well as in space.

(c) Seed production

Plants that produce large numbers of seeds per year tend tobe small in stature, short-lived (i.e. annuals), and producesmall seeds (Moles et al., 2004). Thus, given that high seedproduction is associated with a greater abundance of seedsentering the soil seed bank (Jakobsson, Eriksson & Bruun,2006), and that smaller seeds tend to live longer (seeSection II.3a), it is conceivable that species that typicallyproduce more seeds would exhibit longer seed persistencethan species with lower seed production. However, noevidence for a seed production–persistence trade-off hasyet been found (Bekker et al., 2003; Astegiano et al., 2010),and further research should investigate whether such trade-offs occur within and among species. Modelling also providesa tool for investigating from an evolutionary perspective therelationships and trade-offs between seed characteristics suchas abundance, size, longevity, dormancy and dispersal, andhow they influence ecological fitness in different conditions;while some work has been done in this area (Venable& Brown, 1988; Rees & Westoby, 1997; Kobayashi &Yamamura, 2000), much remains to be investigated.

(3) Genetic diversity

Genetic variation in key characteristics such as longevity,dormancy and antimicrobial properties may confer apersistence benefit on a population or species. Both geneticsand the parental environment (see Section IV) combineto influence seed longevity, dormancy and germinationcharacteristics. Populations with greater genetic diversityin these characteristics may have an advantage in variable



environments as some proportion of their seeds is likelyto germinate and persist across a broader range ofenvironmental conditions. For example, the distributionof seed deaths in time (Kochanek et al., 2011), and thedormancy state of seeds and their sensitivity to naturallyoccurring chemicals (Gorecki et al., 2012), varies within andamong populations. Diversity in dormancy level reducesthe synchronicity of germination; diversity in time of seeddeath, although not necessarily associated with greater seedlongevity (Kochanek et al., 2011), may underpin a bet-hedging strategy that maximises the probability of someseeds surviving in unfavourable climates. Further, low geneticdiversity can lead to inbreeding depression and this has beenassociated with adverse impacts on germination and viabilityin the rare yellow carnation, Dianthus guliae (Gargano, Gullo& Bernardo, 2009). Thus, although yet to be formally tested,it appears that greater genetic diversity, particularly in keyresistance characteristics, may be associated with species thathave more persistent populations.

(4) Phenotypic plasticity

The ability of individual plants to change their growthand physiological responses to their environment, knownas phenotypic plasticity, can influence seed persistence (seeNicotra et al., 2010, for a comprehensive review of plantphenotypic plasticity, including seed traits). Seed traits suchas dormancy (Hoyle et al., 2008b), longevity (Kochanek et al.,2010) and seed size (Kochanek et al., 2011) can vary inmean value and population heterogeneity in response toenvironmental conditions (see also Section IV). For example,cool temperatures during pre-zygotic growth of Wahlenbergiatumidifructa extended the mean longevity of seeds andincreased variation among individuals in one population butnot another (Kochanek et al., 2010). Additional plastic planttraits that may relate to seed persistence include floweringtime (which determines the environment in which seedsdevelop; Donohue et al., 2007), leaf phenology (which canaffect resource accumulation and provisioning to developingseeds) and the production of secondary metabolites aschemical defences (see Nicotra et al., 2010, and referencestherein). Plasticity may not necessarily confer a benefit assome species may be most successful if their seeds arepredominantly long-lived under any conditions. It wouldbe useful to investigate formally whether plasticity is indeedadvantageous in key seed and species traits that are associatedwith longer seed persistence.

(5) Species geography

Patterns in seed longevity and persistence can be associatedwith the native range of species. Species from hot, dryenvironments such as Australia and southern Asia tendto have longer-lived seeds than those from cool, wetenvironments such as Europe (Walters et al., 2005c; Probertet al., 2009). Tropical rainforest species are renowned forhaving short-lived soil seed banks (Vazquez-Yanes & Orozco-Segovia, 1993; Sautu et al., 2006), and this is associated with a

high proportion of rainforest species producing desiccation-sensitive seeds (Tweddle et al., 2003; Berjak & Pammenter,2008); however, this is not always the case, and viable seedsof three pioneer species from a neotropical rainforest inPanama were recovered from topsoil and carbon-dated asbeing 18–38 years old (Dalling & Brown, 2009). Dalling et al.(2011) proposed that seeds with physical dormancy will becommon in environments where microbial pressure is highas they rely on physical protection against soil microbes,whilst seeds with physiological dormancy may be foundacross the range of soil pathogen pressures. Similarly, hardseed coats provide protection against predation, and thusseeds with physical dormancy are more frequently found inhot desert environments where granivory by small rodentsis particularly intense (Paulsen et al., 2013). Further, fire-prone environments may be home to a higher proportionof species for which seeds are encased in woody fruit (seeSection III.6), or which have physiologically dormant seedsthat are triggered to germinate by chemicals found in smoke.However, these hypotheses are yet to be tested.

The extent of distribution of a species can also correlatewith seed bank persistence, but this is not always the case.Among European forest herbs (Van der Veken et al., 2007)and species in the Swiss mountains (Stocklin & Fischer,1999), widely distributed species exhibited more persistentseed banks than narrowly distributed species. However, therewas no such correlation for European woody species (Vander Veken et al., 2007); in this case, other co-variates suchas large seed size and low seed production may be strongerecological drivers of seed persistence.

(6) Alternative seed storage location: the canopy

Whilst the majority of seed-bearing species disperse theirseeds into the soil, a number of species have persistent fruitthat store seeds in the canopy (a strategy known as serotinyor bradyspory) until they are dispersed spontaneously or bya disturbance event such as fire (Cowling & Lamont, 1987).Serotinous species often occur in long-lived woody generasuch as the Myrtaceae, Proteaceae and Pinaceae (Enrightet al., 2007; Menges, 2007; Merritt et al., 2007). An interestingform of serotiny also occurs in the Chenopodiaceae, wherespecies (e.g. Salsola australis) retain seeds in the canopy and theentire plant rolls away, dropping seeds as it goes (Borger et al.,2007). Serotinous seeds are often long-lived in the canopy(Enright et al., 2007; Crawford et al., 2011) and in ex situcontrolled storage (Probert et al., 2009; Crawford et al., 2011),yet they typically do not form a persistent seed bank in the soil(Yates et al., 1995). In the canopy, serotinous seeds experiencefluctuations in ambient temperature and humidity, whichcan lead to ageing and loss of viability (Crawford et al.,2011), and are exposed to predation by insects (Scott, 1982;Lamont & Barker, 1988) and birds (Scott & Black, 1981;Cowling & Lamont, 1987). Serotinous seeds such as thosefrom Banksia (Proteaceae) and Eucalyptus (Myrtaceae) spp. aregenerally non-dormant and typically germinate soon afterthey are dispersed into moist soil (Cowling & Lamont, 1987;Yates et al., 1995). If serotinous seeds do not germinate upon



dispersal, they are likely to lose viability (Weiss, 1984) orsuccumb to predation (Cowling & Lamont, 1987). Thus,given that serotinous seeds are capable of persisting long-term in the canopy and in ex situ controlled storage but notin the soil, it is likely that they exhibit seed traits that affordthem resistance to ageing, but not to germination, predationand microbial decay.

IV. PRE-DISPERSAL ENVIRONMENTALFACTORS

Even before seeds are dispersed from their parent plant,seed persistence traits can be shaped by the environment(Peters, 1982; Ellis, Hong & Jackson, 1993; Finch-Savage &Leubner-Metzger, 2006; Donohue, 2009; Kochanek et al.,2011). The parental environment can affect seed dormancy,germination, size, dispersal, seed coat properties, longevityand fecundity (as reviewed in Roach & Wulff, 1987; Fenner,1991; Donohue & Schmitt, 1998; Gutterman, 2000b; Baskin& Baskin, 2001; Gallagher & Fuerst, 2006; Donohue, 2009)and changes can be imparted at various stages in the lifeof the parent, and even grandparent, plant (Fig. 3). Forexample, seed dormancy and germination can be affected bythe post-zygotic environment as the seed is developing andmaturing on the mother plant (Donohue & Schmitt, 1998),while longevity can also be influenced by changes in the pre-zygotic environment (Kochanek et al., 2011). Dimorphism,a phenomenon where species produce two distinct seedtypes, is also affected by parental environment, with the ratioof the seed types as well as their dispersal and dormancycharacteristics being altered by the environment (e.g. Baker& O’Dowd, 1982; Tielborger & Petru, 2010).

(1) Abiotic influences of the parental environmenton seed persistence

Photoperiod, light quality, water stress, temperature, nutrientsupply and CO2 supply in the parental environment are

abiotic factors that can directly or indirectly influenceseed persistence, and their degree of influence can dependon genetics (Roach & Wulff, 1987; Gorecki et al., 2012).Temperature has the most consistent parental environmenteffect on dormancy, with higher temperatures experiencedby the parent plant leading to less dormant seeds (Roach &Wulff, 1987; Fenner, 1991; Baskin & Baskin, 2001; Steadmanet al., 2004b). The effects of other environmental factorson dormancy and germination tend to be more variable,and depend on the species and the intensity and timingof the environmental stimulus. Longevity can be shortenedby higher parental environment temperatures (Ellis et al.,1993; Kochanek et al., 2011) and drought (Gallagher &Fuerst, 2006), and can also be altered by photoperiod(Contreras et al., 2008) and light quality (Contreras et al.,2009). Seed size and seed coat properties can also varydepending on the abiotic parental environment conditions(as reviewed in Roach & Wulff, 1987; Baskin & Baskin,2001; Donohue, 2009). Fecundity tends to decrease withdrought (Roach & Wulff, 1987) and can also be affected byphotoperiod and light (Gallagher & Fuerst, 2006). Despitethe significant impacts that these abiotic factors can imparton seed dormancy and longevity, plant populations differ intheir sensitivity to environmental fluctuations due to theirdifferent genetic backgrounds (Gorecki et al., 2012).

(2) Biotic stress in the parental environment

Biotic stresses that occur during a seed’s development, such asherbivory or sap removal by insects, predation, plant ageing,and competition for resources between plants or amongseeds within a fruit, can influence a range of persistenceattributes. For example, Baskin & Baskin (2001) list 80 plantspecies where variation in seed size has been attributed tosome of these factors, with defoliation of the parent plantmost commonly causing a reduction in seed mass, andremoval of pods or flowers leading to increased seed massin the remaining seeds. The consequences of altered seedsize as a result of herbivory and predation on characteristics

Fig. 3. Developmental phases of the parent plant in which an environmental effect can be imparted onto the offspring (after Lacey,1996). See also Donohue (2009) for examples of how different plant life histories may interact with parental environments to affectseed characteristics.



such as dormancy are species specific, with both increasesand decreases in seed size leading to higher germinationpercentages, depending on the species (Baskin & Baskin,1988, 2001).

V. POST-DISPERSAL ENVIRONMENTALFACTORS

Once seeds are dispersed, their dormancy, longevity andsusceptibility to predation and decay change over time asmediated by their environment (Finch-Savage & Leubner-Metzger, 2006). Environmental factors that influence seedpersistence after dispersal include the climate, soil and otherfeatures of the site into which seeds are dispersed.

(1) Climatic factors affecting seed persistence

Seed ageing, dormancy, germination, and thus persistenceare all strongly influenced by the moisture and temperatureconditions experienced by seeds.

(a) Temperature, rainfall and humidity

All seeds can equilibrate with environmental temperature,and seeds with water-permeable coats can further equilibratewith environmental moisture (liquid or vapour; Wuest, 2002,2007), these being the two primary factors mediating therate of ageing and dormancy-alleviation reactions (discussedSection II.1a). Higher temperatures can accelerate seedageing (Ellis & Roberts, 1981) and alleviate physical (Baskin,2003) and physiological dormancy (Iglesias-Fernandez et al.,2011) in the laboratory. In the field, seeds in strongly seasonalclimates can experience daily and seasonal fluctuationsin temperature and moisture, particularly in the uppercentimetres of soil (Benvenuti, MacChia & Miele, 2001;Merritt et al., 2007; Saatkamp et al., 2011a). Exposure toreduced rainfall and more stable temperatures affords longerpersistence in desiccation-tolerant seeds (Burnside et al.,1996), whilst exposure to dry climates can kill desiccation-sensitive seeds (Tweddle et al., 2003).

Quantification of the moisture and temperature conditionsexperienced by seeds over time (hydrothermal time) maybe used as an informative correlate for predicting seedpersistence (Iglesias-Fernandez et al., 2011). In general, lowerhydrothermal time during in situ burial correlates with longerseed persistence (Davis et al., 2005), and greater hydrothermaltime following dispersal favours more rapid dormancyalleviation (Steadman, Crawford & Gallagher, 2003; Meyer& Allen, 2009). However, most hydrothermal time studieshave used species that lose physiological dormancy via dryafter-ripening, thus the relationship between hydrothermaltime and persistence or dormancy may depend on thespecies and its dormancy alleviation requirements. Althoughthe embryos of physically dormant seeds are protectedfrom experiencing moisture fluctuations by their water-impermeable seed coats, extended exposure to warm, wet

conditions can weaken the seed coat and render the seedsnon-dormant (van Klinken et al., 2006; Turner et al., 2009).Moreover, there may be optimal amounts or thresholds ofhydrothermal time beyond which dormancy is re-induced.Thus further research is needed to assess the generalityof any relationships between hydrothermal time and seedpersistence.

(b) Wet-dry cycles: a special case

Rain events alternating with dry periods can influence seedgermination, dormancy, longevity and thereby persistence inboth agricultural and natural systems, including temporarywetlands (Brock, 2011). Moisture fluctuations in soils canpromote seed germination by priming non-dormant seeds(Gonzalez-Zertuche et al., 2001) and by actively alleviatingphysiological dormancy (Hoyle et al., 2008a; Long et al.,2011b), most likely through changes to the concentrationof, or sensitivity to, dormancy-regulating hormones in theseed (Long et al., 2010). Wet-dry cycling can also extend seedlongevity by restoring antioxidant capacity and thereforestress tolerance and ability for self-repair (Long et al., 2011a).Even daily fluctuations in humidity can lead to seedrepair, particularly for seeds with mucilaginous wings thatcan absorb water from dewfall (Huang et al., 2008). Theextent to which increasing the number of wet-dry cyclescan continue to impart dormancy-alleviating and longevity-extending effects is not clear, but may be around three or fourcycles, and depend on the extent of accumulated damageprior to rehydration (Butler et al., 2009). At some point, seedphysiological repair systems will reach exhaustion (reviewedin Kranner et al., 2010) and more research is needed tounderstand the thresholds and mechanisms through whichwet-dry cycling influences seed persistence.

(c) Future climates

Predictions of future climate scenarios are complex, andwhilst they are likely to involve warmer climates andmodified rainfall, local changes will vary greatly indirection, magnitude and seasonality (Solomon et al., 2007).Furthermore, the spatial and temporal rates of these changeswill be highly variable across ecosystems (Burrows et al.,2011). The impact that these changes have on seedpersistence will be a function of location and species (Walcket al., 2011; Ooi, 2012). The warmer and drier conditionsthat are most commonly predicted are likely to promotemore rapid dormancy loss in winter annuals, but preventdormancy alleviation (or induce secondary dormancy) inspecies requiring cold-stratification (Walck et al., 2011).Such changes in climate may alter the species balancein plant communities, particularly affecting annual species(Kimball et al., 2010). Species may adapt to future climatesvia selection of adapted individuals, rapid microevolution,phenotypic plasticity, and by communicating informationabout environmental conditions between generations viaepigenetic and parental environment effects (Parmesan,2006; Richards, Bossdorf & Pigliucci, 2010; Hoffmann &



Sgro, 2011). Certain species may fail to adapt and thusdecline in abundance and range, in some cases leading tolocalised extinction.

(2) Soil factors affecting seed persistence

The physical, chemical and biological properties of soilscombine with climate and with seed characteristics suchas the permeability and antimicrobial characteristics of theseed coat to influence when and how seeds exit the soil seedbank (Davis, 2007; Dalling et al., 2011; Pakeman, Small &Torvell, 2012). The effects of soils on seeds are typicallyinvestigated using field-based seed burial trials, but of themany reports in the literature, few present comprehensivedetails of the soil conditions; a factor that is identified asa driver might therefore be confounded by other factorsthat were not measured. Nevertheless, here we discuss thesoil characteristics that may have a direct impact on seedpersistence.

(a) Physical

Soil temperature, water potential and light transmissibilityaffect seed persistence through their influences ongermination, dormancy and ageing. Soil temperature isinfluenced by soil colour, soil texture, and climate (e.g.darker soils tend to absorb more heat; Long et al., 2009),while texture and bulk density affect water potential andlight transmissibility (Mandoli et al., 1990; Brady & Weil,1999). Lower soil temperature and water availability promotepersistence of desiccation-tolerant seeds (Arachchi, Naylor &Bingham, 1999; Long et al., 2009; Pakeman et al., 2012)by providing conditions that minimise seed ageing anddormancy loss (Davis et al., 2005) and microbial activity(Schafer & Kotanen, 2003). Well-drained sandy soils dry outmore rapidly than silt or clay soils, so wet-dry cycles mayoccur more frequently but to a lesser amplitude in sandysoils, potentially extending seed longevity and overcomingdormancy (Long et al., 2009, 2011a,b). Not unexpectedly,moist soils are likely to be critical for even short-term survivalof desiccation-sensitive species (Tweddle et al., 2003).

(b) Chemical

The chemical properties of soils, including nutrient content,organic matter and pH, can affect seed persistence throughtheir effects on soil water-holding capacity (influencing seedageing, repair and dormancy), nitrate content (dormancyalleviating) and, most importantly, microbial activity (causingseed decay). A study by Bekker et al. (1998b) tested thehypothesis that enhanced inorganic nutrient availabilityfavours soil biota and decomposition processes that decreaseseed longevity in the soil. Fertiliser applications of nitrogen,phosphorus and potassium to five sites across the Netherlandsand England did not alter the seed persistence of 17 fen-meadow species, despite affecting the standing vegetation.However, a correlative study of natural soil conditions andseed persistence showed that soils with lower carbon:nitrogen

ratios (i.e. with a smaller pool of carbon to support microbialgrowth) can favour longer seed persistence (Pakeman et al.,2012). Similarly, in an experiment in which three differentsoils were introduced to a single site, seed persistence of threeweed species was shortest in the soil with the highest organicmatter content, phosphorous content and cation exchangecapacity (Long et al., 2009). The pH of soils can furtheraffect nutrient availability for plants and microbes, withgreater acidity and alkalinity being associated with shorterseed persistence (Long et al., 2009; Pakeman et al., 2012).Finally, salinity can limit germination by reducing the waterpotential of the soil solution to below the threshold waterpotential for a species. Thus soil chemical properties canvary considerably across landscapes and contribute to thevariation in seed persistence within a species.

(c) Gaseous environment

The gaseous environment in soils can differ from theatmosphere above, and is affected by soil structure,hydrology, and the level of microbial activity. Gases thatinfluence germination and dormancy include oxygen, carbondioxide, nitrous oxide and ethylene. The concentration ofthese gases can differ among localities and depths in the soilprofile due to fire, respiration from neighbouring organisms,and microbial breakdown of organic matter (Sheppard &Lloyd, 2002; Nelson et al., 2012). Seed responses to thegaseous environment differ greatly among species, anddepend on the dormancy state of the seeds and on thebalance of gases present. Variation in the balance of gases caninform seeds about their burial depth, the time of year, andthe presence of plant competitors. Fundamentally, oxygen isrequired for seed respiration and the progress of germination(Al-Ani et al., 1985); in the hypoxic or anoxic environmentof water-logged soils, germination is inhibited and secondarydormancy can be induced in some species (Corbineau, 2012).Carbon dioxide levels increase with soil depth, can follow anannual cycle in response to microbial activity, and increasein the presence of respiring roots (Baskin & Baskin, 2001).Other gases such as ethylene and nitrous oxides that alleviatedormancy and induce germination may be more abundantafter fire and cue germination at a time when competitionis low (Bradshaw et al., 2011; Nelson et al., 2012), whileother volatile organic compounds from smoke may inhibitgermination (Pennacchio, Jefferson & Havens, 2007). Thus,the soil atmosphere can play a critical role in informingseeds about their environment, thereby influencing seedpersistence.

(d ) Biological

Although microbial activity can drive seed mortality in soils,as described above, soil microbes are diverse and so are theirinteractions with seeds, as reviewed in Chee-Sanford et al.(2006) and Wagner & Mitschunas (2008). For example,the soil fungus Fusarium oxysporum can infect and decayhealthy seeds (Thomas et al., 1999), whilst the collembolanProtaphorura fimata predates upon seed-rotting microbes and



acts as a seed protectant (Mitschunas, Wagner & Filser, 2006).Certain seed-surface-associated bacteria, too, have disease-suppressive properties that prevent infection and decay bypathogenic species (Nelson, 2004). Soil microbes can be anintegral part of seed germination, breaking down the seedcoat so that germination can occur (van Leeuwen, 1981;Morpeth & Hall, 2000; Delgado-Sanchez et al., 2011), anddegrading allelochemicals in the soil that would otherwiseinhibit germination (Zhu, Zhang & Ma, 2011). Both fungiand bacteria in the soil can be attracted to seeds in responseto seed exudates, and infection therefore tends to occurduring imbibition and germination (Nelson 2004). Asidefrom the direct impacts of soil microorganisms on seedpersistence, fungal activity is responsible for the non-wettingcharacteristics of some soils, and thus has indirect impactson seed ageing, dormancy and germination by altering thewater-holding characteristics of soils (Franco et al., 2000).

(3) Other site-related environmental factorsaffecting persistence

The persistence of seeds in a particular soil and climatecan be further altered by site-specific factors such as light,disturbance and the presence of animal dispersers andpredators.

(a) Light

The photoperiod, quality and intensity of light in thepost-dispersal environment can influence seed dormancyalleviation and germination timing (Long et al., 2011b;Saatkamp et al., 2011b; Corbineau, 2012), sensitivity todormancy-breaking chemicals (Long et al., 2011b), andageing (Huang et al., 2008; Roqueiro et al., 2010). The effectsof alternating light/dark conditions on dormancy alleviationand germination are well described for many species (Wesson& Wareing, 1969; Pons, 2000; Saatkamp et al., 2011b), butit is not clear whether seeds perceive seasonal subtleties inphotoperiod in the same way as do parental plants (seeSection IV). Seeds at or very near the soil surface receivedirect or filtered sunlight, the intensity and quality of whichdepend on the degree of filtering due to soil, canopy and cloudcover, and geographical factors such as latitude and altitude(Anderson, 1964). The depth of light penetration into soil(ranging from as little as < 1 mm to > 1 cm) depends on thesoil type, grain size and composition, but is typically negligible(Mandoli et al., 1990; Ciani, Goss & Schwarzenbach, 2005).Filtering of sunlight by a leaf canopy results in seeds onthe soil surface receiving light enriched in green and far-redwavelengths (Batlla, Kruk & Benech-Arnold, 2000), whilstcompounds within the seed coat or endosperm, such aschlorophyll, anthocyanins and carotenoids, and the textureof the seed coat itself, can also influence the quality of lightperceived by the embryo (Hendricks, Toole & Borthwick,1968; Widell & Vogelmann, 1985; Goggin & Steadman,2012). Ultraviolet light can damage seeds through membranedeterioration and perturbation of the antioxidant defencesystem (Musil, Newton & Farrant, 1998).

(b) Disturbance

Natural, agricultural and industrial disturbance to soils canalter the persistence of seeds by changing the temperature,moisture, gas and light conditions to which they are exposed.Species that are adapted to disturbed environments typicallyexhibit more persistent seed banks than do species fromstable habitats (Thompson et al., 1998; Holzel & Otte, 2004).Key natural disturbances that are predicted to alter seedpersistence are fire (Nelson et al., 2012), flooding (Geissler& Gzik, 2008), erosion (García-Fayos, Bochet & Cerda,2010) and grazing (Darabant et al., 2007). Seeds exposeddirectly to fire may combust or be killed by its heat, butthe heat, chemicals and improved light conditions in apost-fire environment can also promote seed germination(Nelson et al., 2012). Fire may also degrade allelochemicalsderived from surrounding vegetation that otherwise inhibitgermination (Preston & Baldwin, 1999). Flooding altersthe light and gaseous environment that seeds experience,and may facilitate burial in the soil profile. In agriculturalcontexts, tillage buries some seeds and brings others to thesurface, and the resultant changes in light, temperatureand moisture conditions thereby affect seed dormancyand germination (Jensen, 1995; Anderson, 1998). Similarly,mining operations that remove and stockpile topsoil alterthe distribution of seeds in the soil profile (Johnson & West,1989; Koch et al., 1996; Bond & Grundy, 2001).

(c) Burial depth

Seeds can migrate to different depths in the soil profile dueto natural soil movement and rain (Benvenuti, 2007a), tillage(Roger-Estrade et al., 2001), caching by animals (Steele,2008), and by the action of contractile roots (e.g. Emexspinosa; Evenari, Kadouri & Gutterman, 1977), stolons (e.g.Trifolium subterraneum; Smetham, 2003) and hydroscopic awns(e.g. Erodium spp.). The depth at which seeds are buried caninfluence seed persistence, with seeds typically persistinglonger at greater depths (Weiss, 1984; Miller & Nalewaja,1990). As depth increases, light is excluded (Mandoliet al., 1990), and temperature (Saatkamp et al., 2011a) andmoisture conditions become more stable, generally slowingthe processes of dormancy release and ageing (outlinedabove). Seed persistence is further favoured at depth giventhat soil burial can protect seeds from predation (Hulme,1998a) and the passage of fire (Weiss, 1984; Hodgkinson &Oxley, 1990). Whilst the ability to emerge successfully fromdepth may be favoured among larger seeds due to their largerstorage reserves (Harper, Lovell & Moore, 1970; Grant et al.,1996), seeds of all sizes may germinate at depth and fail toemerge (a phenomenon known as suicidal germination), thusterminating their persistence in the soil seed bank (Benvenutiet al., 2001; Saatkamp et al., 2011a).

(d ) Toxic and dormancy-breaking chemicals

Chemicals in the environment can alter seed persistenceby alleviating dormancy and inducing the completion of



germination, by inhibiting germination and by killing seedsthrough direct toxic effects. Allelopathic chemicals fromleaves and roots can leach into the soil profile and inhibitgermination, as has been demonstrated for many speciesincluding the Mediterranean shrub Cistus ladanifer (Sosa et al.,2010) and a range of Poaceae species (Kato-Noguchi &Macías, 2008). Hormones can be exuded by roots of adultplants into the soil and may inhibit germination (e.g. abscisicacid: Zhao et al., 2011a) or alleviate dormancy and inducecompletion of germination (e.g. strigolactones and ethylene,acting on parasitic species: Logan & Stewart, 1991; Matusovaet al., 2005). Seeds themselves can exude chemicals thatinfluence the germination of neighbouring seeds (see SectionII.3e). Another way in which chemicals enter the environmentis through fire, which can introduce stimulatory chemicalssuch as karrikins, cyanohydrins and potentially nitrous oxidesinto the soil (Nelson et al., 2012). The germination responseto these smoke-derived chemicals depends on the species, aswell as the dormancy and hydration state of the seeds at thetime that the signal is perceived (Long et al., 2010, 2011b,c). Inagricultural systems, use of non-selective herbicides prior tosowing the crop can select for higher weed seed dormancy byonly removing the early-germinating cohort of the weed seedbank (Owen et al., 2011). Collectively, therefore, chemicalsinfluence the timing of germination by communicatinginformation about the availability of resources and potentialcompetitors in the surrounding environment.

(e) Modification by dispersal agents

Dispersal influences seed persistence through the mechanicaland chemical processing of seeds and by determiningwhere seeds are deposited. Although seeds and fruits mayexhibit morphologies that are conducive to dispersal bya particular mechanism, most species are dispersed bymultiple means, including via animals, wind, water, gravityand ballistics (Bakker et al., 1996). Seed persistence canbe modified by the removal of fleshy fruit tissues duringdispersal by animals, as these tissues can contain secondarymetabolites that inhibit germination and carbohydratesthat influence the subsequent microbiological environmentof the seed (Robertson et al., 2006; Traveset et al., 2007).Other seed modifications that arise during dispersal includechemical and physical scarification sustained during gut-passage or movement in the environment, which canlead to earlier germination (Traveset et al., 2007; Gross-Camp & Kaplin, 2011). Some caching seed predators buryseeds in conditions that favour germination, whilst squirrelsmanipulate seeds so that germination is delayed or prevented,thus facilitating long-term storage (Steele, 2008; Xiaoet al., 2009).

The context in which seeds are deposited is also influencedby the dispersal mechanism. When dispersal is non-randomin destination, the conditions experienced at depositionsites may predictably modify persistence (Schupp, Jordano& Gomez, 2010). Two examples are: vertebrate-dispersedseeds, which may be deposited with faecal material that canshorten or extend the time to germination depending on its

chemical composition (Marambe, Nagaoka & Ando, 1993;Bradford & Westcott, 2010); and the deposition of seeds bywatercourses into particular fluvial environments dependingon the hydrodynamics and seed morphology (Merritt &Wohl, 2002).

(f ) Post-dispersal predation

Post-dispersal seed predation is a primary determinant ofseed persistence in both natural and managed systems(Hulme, 1998a; Marino et al., 2005; Bruun et al., 2010). Afterdispersal, seeds are typically found above ground wherethey encounter the threat of predation by generalist animals[reviewed in Janzen (1971) and Hulme (1998b)] includingbirds, mammals, insects and earthworms (see also Sallabanks& Courtney, 1992; Regnier et al., 2008; Forey et al., 2011).Post-dispersal predation is often rapid and kills a significantproportion of seeds (Blate et al., 1998; Rodriguez-Perez &Traveset, 2007; Gonzalez-Rodriguez & Villar, 2012; Salazaret al., 2012). However, rates of predation vary with differenthabitats (Gonzalez-Varo, Nora & Aparicio, 2012; Salazaret al., 2012), through time (Yoko-o & Tokeshi, 2012) and withfactors such as habitat management and burning (Taskeret al., 2011). This makes post-dispersal seed predation aninfluential filter for recruitment and ultimately for dynamicsof plant abundance (Hulme & Hunt, 1999) and distribution(Calvino-Cancela, 2007), seedling community composition(Paine & Beck, 2007), colonisation and invasion (Ferreras& Galetto, 2010). While post-dispersal predation can havesignificant impact this will only happen if recruitment is seed-limited (Calvino-Cancela, 2007). The factors influencingpost-dispersal predation are both intrinsic (see SectionII.3a–e) and extrinsic to the seed, as discussed here.

Factors extrinsic to the seed that influence post-dispersalpredation are varied. Crop size or seed density at thedeposition site can be influential. Dispersal that removesseeds from the vicinity of the parental or conspecific treesmay remove those seeds from highly competitive situationsand specialist predators and pathogens, thereby enhancingtheir survival (Janzen, 1970; Connell, 1971). While somestudies have supported this idea (e.g. Paine & Beck, 2007)others have found no effect (Marino et al., 2005), that theeffect of predator preferences for particular species dominates(Hulme & Hunt, 1999) or that it is dependent on the scaleof investigation (Blendinger & Diaz-Velez, 2010). However,when predator densities have an upper limit, high seeddensities can result in faster predator satiation and thusincreased survival (Perez-Ramos & Maranon 2008; Fadiniet al., 2009; Bagchi et al., 2011; but see Sun et al., 2007; Lucas-Borja et al., 2012). By contrast, where predator densities canrespond to seed availability, high seed densities can resultin higher predator densities and therefore predation (Zonget al., 2010) – a situation that appears more common forinvertebrate predators (Forget, Kitajima & Foster, 1999;Espelta et al., 2009).

Irrespective of seed density, the species composition of theplant community and the seed bank at the deposition sitewill influence the relative attractiveness of a seed to predators



while the composition of the local predator/parasitoidcommunity, and interactions between these (Bonal &Munoz, 2007) will determine the suite of species whoseseeds experience the greatest predation (Christianini &Galetti, 2007). Seed predation rates will also be influencedby microsite conditions that influence the behaviour andabundance of predators such as canopy and vegetationcover (Perez-Ramos & Maranon, 2008; Sanguinetti &Kitzberger, 2010), habitat type (Rodriguez-Perez & Traveset,2007), landscape context, e.g. fragmentation and edgeeffects (Fleury & Galetti, 2006; Craig, Orrock & Brudvig,2011; Doust, 2011; Gonzalez-Rodriguez & Villar, 2012;Gonzalez-Varo et al., 2012) and disturbance (Taskeret al., 2011).

Seed handling by both dispersers and predators is alsoinfluential in determining seed fate, and different handling,even by the same species of disperser, can result in verydifferent outcomes. For example Gross-Camp & Kaplin(2011) found that primates process seeds in different ways,deposit them in different ways and in different environmentalcontexts, and that these differences resulted in variable ratesof seed persistence, predation and establishment. Removal offlesh and the burial of seeds by dispersers has been shown toreduce predation rates in some contexts (Andresen & Levey,2004; Jansen et al., 2010; Beaune et al., 2012). However,this may come at a cost as seeds passing through the gutof frugivores are deposited with dung adhering to themand this can increase detection and predation (Andresen &Levey, 2004), an effect that can be modified by the identityof the species producing the dung (van Klinken & White,2011). The pattern of deposition can also influence survivalwith clustered deposition of seeds in dung often increasingthe probability of discovery and consumption by predators(Russo, 2005; Velho, Datta & Isvaran, 2009; but see Bradford& Westcott, 2011).

While interactions between seeds and predators are usuallyto the predator’s benefit rather than the seed’s, predators arenot always efficient and seed death is not always guaranteed.Many dispersers and seed predators cache and store seedsfor later consumption, sometimes in vast numbers, and theircaching practices may inadvertently promote persistenceby limiting exposure to further predation (Regnier et al.,2008). A number of seed-caching predators prune embryosfrom seeds to prevent or delay germination of stored seedsand this in turn has resulted in some plants evolvingregeneration strategies to counter this (Cao et al., 2011).For example, plants may escape partial predation throughrapid germination responses, effectively converting energystores into less digestible taproots and stems (Hadj-Chikh,Steele & Smallwood, 1996; Chang, Xiao & Zhang, 2009).Further, caches of seeds with impermeable seed coats aremore likely to escape discovery because the olfactory cuesthat animals use to detect buried caches are not releasedby dry seeds (Paulsen et al., 2013). Thus the interactionsbetween seeds and predators are complex, with intrinsicseed and species factors and extrinsic environmental factorsinfluencing predation outcomes.

VI. INTEGRATING AVAILABLE KNOWLEDGEINTO A PREDICTIVE MODEL OF SEEDPERSISTENCE

An improved understanding of seed persistence and acapacity to predict it will enhance the management ofplants in agricultural, natural and restored systems. Wewill need to identify the drivers of seed persistence andunderstand how they interrelate so that seed persistencecan be predicted under particular conditions. Conceptual,empirical and integrative simulation models will all play arole in this process.

(1) The resistance–exposure model

As highlighted in this review, no one factor is capableof predicting seed persistence, not even under ex situ dry-storage conditions, and in real situations many factors arelikely to have an effect (Golovina et al., 2010). To helpaddress the need for predicting how seed, species, climate,soil and other site factors influence overall seed persistencein a wide range of contexts, we propose the developmentof a general resistance–exposure model (Fig. 4). The modelassumes that the persistence of a given seed is bounded bythe potential persistence of that seed under ideal conditions.This potential persistence is then reduced by exposure ofthe seed to relevant risk factors, to which that seed has acertain level of ‘resistance’. In other words, the persistenceof a given seed population in the field will depend on (i)its maximum persistence, (ii) its exposure to environmentalconditions conducive to germination, ageing, predation anddecay, and (iii) its intrinsic resistance to those fates.

To estimate maximum persistence for ideal conditions(e.g. in a conservation seed bank at −20◦C and 15% RH),seeds could be subjected to a controlled ageing test forwhich results have been calibrated to estimate maximumlifespan, following the work of Ellis & Roberts (1980). Thiswould involve placing seeds under a standardised set oftemperature and humidity conditions that accelerate ageing(e.g. sustained storage at 60% RH and 45◦C; Davies &Probert, 2004); the time taken for half the population to diewould be used to estimate its potential persistence in otherconditions, based on an underlying correlation in persistenceunder these different conditions (Long et al., 2008; Probertet al., 2009). To this assessment of the potential persistence,which represents the species’ inherent genetic resistance toageing, details of other key resistance and exposure factorscould be overlaid to derive a final estimate of persistence for aparticular seed population and site. This process is illustratedin Fig. 4B, where the maximum persistence of a hypotheticalseed population is 10 years according to the controlled ageingtest. This estimate may be reduced to 1 year if the targetsite is warmer and wetter than the ideal conditions, giventhe potential for increased ageing and microbial attackunder these conditions, but the presence of antimicrobialcompounds or disease-suppressing microorganisms in oron the seeds may afford them some resistance such that



Fig. 4. (A) The resistance–exposure model: the challenge of predicting seed persistence in different environments can be resolvedby understanding how the resistance of seeds interacts with exposure to environmental factors that favour seed germination, ageing,predation, decay and death. (B) An example of the resistance–exposure model applied to an hypothetical seed population; maximumseed persistence may be estimated at 10 years according to the controlled ageing test, but reduced to 2 years once soil, climate andsite conditions are accounted for, along with seed characteristics such as antimicrobial compounds that afford resistance to decay.

the estimated persistence is 2 years. The next steps indeveloping this resistance–exposure model are: (i) calibratethe controlled ageing test to predict persistence under idealconditions, (ii) identify the key drivers of resistance andexposure among the many factors discussed herein, and(iii) quantify the impact of those key drivers for a range ofimportant species and situations. The model may then betested for its applicability to a range of species and habitats,and its strengths and limitations assessed.

Many sophisticated simulation models have beendeveloped to predict weed population dynamics, and theseincorporate some components of seed persistence (e.g.Forcella, 1993; Grundy, Mead & Burston, 2003; Colbachet al., 2006, for reviews see Colbach & Debaeke, 1998;Forcella et al., 2000; Grundy, 2003; Holst, Rasmussen &Bastiaans, 2007). These tend to focus on agricultural systems,and particularly the ways that management practices, suchas tillage, and the soil environment affect germination (oremergence) and thus competition with the crop (Benech-Arnold et al., 2000; Colbach et al., 2005; Batlla & Benech-Arnold, 2007). They have tended to represent a single speciesor a few specific dominant species, although some morerecent models represent multiple species with the flexibilityto include new species relatively easily (e.g. Renton, Diggle& Peltzer, 2008; Parsons et al., 2009; Gardarin, Durr &Colbach, 2012). Our proposed general resistance–exposuremodel differs from these models in focussing on seedpersistence rather than general population dynamics, andon the full range of factors likely to influence persistencein both natural and agricultural systems rather than theclimatic and management factors likely to be of primeimportance in agricultural systems. The main purpose ofthe resistance–exposure model is to help estimate the likelypersistence of seeds in the absence of replenishment, e.g.to inform management aimed at eradication or significantreduction of seed banks, while the main purpose ofagricultural weed population simulation models is to predict

how weed populations will change over time, with seedbank persistence a secondary concern. Nonetheless, thegeneral resistance–exposure model could help to informsome components of weed population simulation models, asexplained below.

(2) Applications for improved predictive modellingof seed persistence

The resistance–exposure model can be applied to predictpersistence of both desiccation-tolerant and -sensitive seedsin a range of ex situ and in situ environments, given thatthe inherent persistence attributes of seeds are incorporatedinto the resistance component, and the degree to which theenvironment favours persistence or demise is encapsulatedby the exposure component. Estimates of seed persistencearising from the model could be used to guide themanagement of plant species in agricultural, natural andrestored systems, or to inform other agricultural, biologicaland ecological models of processes that are influenced by seedpersistence. Seed persistence estimates could help to designoptimal seed bank management regimes to benefit nativespecies and hinder invasive species, informing the weederadication planning model proposed by Panetta et al. (2011),for example. Further, seed persistence can delay germination,and this has a knock-on effect for the time to adult plantmaturity, which is a key determinant of the likelihood ofa plant species surviving in different fragmented landscapesunder a changing climate (Renton, Shackelford & Standish,2012). Simulation models of agricultural weed populationdynamics, such as those mentioned above, can be used to (i)help develop practical weed management strategies, (ii) act asthe basis of computer decision-support tools (Forcella, 1998;Holst et al., 2007; Renton et al., 2008; Parsons et al., 2009), (iii)predict the evolution of herbicide resistance (Neve et al., 2003;Thornby & Walker, 2009; Renton et al., 2011), and (iv) assistin analysing complex economic trade-offs between different



weed management strategies in agricultural systems (Pannellet al., 2004; Benjamin et al., 2009; Lawes & Renton, 2010;Renton, 2011). The usefulness of these models will dependon the accuracy of the estimates of seed persistence on whichthey are based, particularly when the long-term dynamics ofseed banks are an important part of the system. These types ofmodels have generally focused on accurately predicting seedgermination and emergence, but our proposed persistencemodel may help to improve the mortality sub-models bysynthesising all available information that is likely to affectseed mortality over time. Thus, by improving the abilityto rapidly and accurately predict seed persistence in aquantitative way, the resistance–exposure model – usedalone, or in support of other models – will facilitate strategicmanagement of both desirable and invasive species in ournatural and agricultural landscapes.

VII. CONCLUSIONS

(1) Seed persistence is a complex expression of seed andspecies characteristics that are altered by the environment.Seed and species characteristics contribute to a seed’sresistance to germination or death, whilst exposure tothe climate, soil and other site characteristics of a seed’spre-dispersal and post-dispersal environment ultimatelydetermine when and how seeds germinate or die.

(2) Seed dormancy, longevity, and defence characteristicsall contribute to a seed’s ability to resist exiting the soilseed bank.

(3) Abiotic and biotic conditions in the pre-dispersal(parental and grandparental effects) and post-dispersalenvironments can alter seed dormancy, longevity andgermination characteristics.

(4) Future studies of seed and species characteristicsrelating to seed persistence need to identify which traits drivepersistence by conferring resistance to germination, ageing,predation and decay in a range of environmental conditions.In doing so, we will be able to identify phylogenetic trendsin persistence, and advance towards the development of aquantitative resistance–exposure model for predicting seedpersistence.

VIII. ACKNOWLEDGEMENTS

This collaboration was supported by a Rural IndustriesResearch and Development Corporation National Weedsand Productivity Research Program Grant (PRJ 006918)and financial assistance from The University of WesternAustralia’s Faculties of Sciences for the Seed PersistenceWorkshop (October 2011). We thank Dane Panetta (Queens-land Government) and Krishnapillai Sivasithamparam (TheUniversity of Western Australia) for helpful discussions onseed persistence. We also thank two anonymous reviewersfor their detailed suggestions for improving this review.

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(Received 27 February 2013; revised 30 January 2014; accepted 4 February 2014 )


The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise

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