Seeds Ecology, Biogeography, and Evolution of Dormancy and Germination To Drs. Lela Viola Barton and Marianna Georgievna Nikolaeva, two ladies who distinguished themselves by their contributions to our knowledge of seed germination biology Seeds Ecology, Biogeography, and Evolution of Dormancy and Germination Second Edition Carol C. Baskin Jerry M. Baskin Department of Biology University of Kentucky Lexington, Kentucky, USA AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON(cid:129)NEWYORK(cid:129)OXFORD(cid:129)PARIS SANDIEGO(cid:129)SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO AcademicPressisanimprintofElsevier AcademicPressisanimprintofElsevier 525BStreet,Suite1900,SanDiego,CA92101-4495,USA 32JamestownRoad,LondonNW17BY,UK 225WymanStreet,Waltham,MA02451,USA Copyrightr2014ElsevierInc.Allrightsreserved. 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BritishLibraryCataloguing-in-PublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress ISBN:978-0-12-416677-6 ForinformationonallAcademicPresspublications visitourwebsiteatelsevierdirect.com TypesetbyMPSLimited,Chennai,India www.adi-mps.com PrintedandboundintheUnitedStatesofAmerica 14 15 16 17 18 10 9 8 7 6 5 4 3 2 1 Preface to the Second Edition Since the publication of the first edition of our book on physiological dormancy, with which she did agree. We seeds in 1998, we have continued to learn about seed exchangedbookswithherandstillhavethegiftcopyofher germination ecology, and new information has come from book titled Reference Book on Dormant Seed Germination manysources.InanattempttohelpfillavoidinSeedswith (published in Russian in 1985). If you use Nikolaeva’s respecttoinformationontropicalmontanespecies,wehave formula system for seed dormancy classification, this book studied about 50 species from Hawaii (USA). This work has a wealth of information about dormancy, especially for was made possible in large part thanks to the great efforts species from Russia and northern Europe. We also have of Alvin Yoshinaga (Lyon Arboretum, University of benefited greatly from meetings of the International Seed Hawaii)whocollectedseedsofmanyspeciesandhelpedus Science Society (ISSS) and in particular the International in many ways. Graduate students (Christopher Adams, SeedEcologymeetings,whichwerecosponsoredbyISSS. NalinGama-Arachchige,TracyHawkins,SitiNurHidayati, A major source of new information has been from the Gehan Jayasuriya, Xiaojie Li, Xiaoxia Qu, Adriana Sautu published literature on seeds. Thanks to increased use of and Jeffrey Walck) in our lab during the post-Seeds period the web and computers, it has become much easier to have done detailed studies on germination of various find new information about seeds, i.e., no more looking species. It has been our privilege tohost visitorsin our lab through massive hardbound volumes of Biological fromChina,SpainandTaiwanandtocollaboratewithseed Abstracts because abstracts are available on-line via the scientistsinAustralia,Belgium,China,England,Germany, library. Also, it is much easier to obtain copies (or pdf India, Iran, Israel, Japan, Mexico, Spain, Sweden, Sri files) of papers than it was in the 1970s, 1980s and early LankaandTaiwanonstudiesonmanyinterestingspecies. 1990s when you ordered a reprint by writing the author a Also, we have visited seed scientists in Australia, China, letter or postcard and waited up to many weeks for it to England, Greece, India, Israel, Japan, Malaysia, Mexico, arrive. Further, being able to access a large number of New Caledonia, Panama, Sweden, Sri Lanka and Taiwan. journals from South America, in particular Brazil, and We have learned much from many people and appreciate other parts of the world on the computer/web is a allthehelp. modern-day miracle. Also, it is now relatively easy to Since publication of Seeds in 1998, we have visited have a good understanding of the seed germination litera- mainland China 11 times and established ongoing ture from China. Most papers being published in Chinese collaborative projects with Professor Dun-Yan Tan and now have an English abstract, and tables and figures are Dr. Juan-Juan Lu at Xinjiang Agricultural University in in English. Furthermore, many studies done on seeds in Uru¨mqi, Xinjiang Province, on species of cold deserts. ChinaalsoarebeingpublishedinEnglish. We also have greatly enjoyed working with and interact- The result of all the new contacts and collaborations ing with many people in China, including Professors Min with other seed scientists and the increased easiness with Cao, Xishuangbanna Tropical Botanical Garden, Yunnan which papers on seeds could be obtained led to a massive Province; Guo-Zhen Du, Lanzhou University, Gansu accumulation of literature in our lab. Finally, in autumn Province; Yan-Rong Wang, Lanzhou University, Gansu 2005 we decided that the time had come to sort, synthe- Province; and Zhen-Ying Huang, Chinese Academy of size and then to greatly expand and in some cases rewrite Science,Beijing,andtheirmanytalentedstudents. large portions of Seeds in an effort to accommodate Another source of new information has been through the new information. However, the goal for the second email contacts with other people. From 2000 to 2005, we edition is the same as it was for the first edition: that is, exchangedanumberofemailswiththelateM.G.Nikolaeva we want to provide the reader with a comprehensive and greatly enjoyed learning her opinions on smallembryos overview of the ecology, biogeography and evolution of in Martin’s dwarf seeds and on our placement of her seed dormancy and germination. Working on the revision “mechanicaldormancy”andher“chemicaldormancy”under of Seeds has been challenging but informative and xi xii PrefacetotheSecondEdition enjoyable,andwe hopereadersalsowillbeeager tolearn the great efforts of Patricia Gonzalez, Melissa Read, more about this remarkable stage in the life cycle of seed Carol Lewis, Susan Stuart, Liz MacSween, Glnys plants. NorquayandotherElsevierstaff.Wearegratefulfortheir After the manuscript for a book has been submitted to careful, patient and highly competent attention to the fine the publisher, a huge amount of work must still be done, details and for their good cheer throughout the whole and our book would never have been completed without process. Preface to First Edition Our involvement in seed germination began in spring wetlands.However, some seedshavecome from species of 1966, when, as graduate students at Vanderbilt University deserts (New Mexico and Arizona), mountains (Colorado in Nashville, Tennessee (USA), we took a course in plant and Utah) and semi-arid habitats (Texas and Utah) in autecology under Professor Elsie Quarterman. She came western USA. To expand our knowledge of the field, we to class one day with a list of research projects and went have made great efforts over the years to become familiar around the room assigning one of them to every two with,andcollectcopiesof,thepastandcurrentliteratureon students. We happened to be sitting next to each other, seedgerminationecology. and thus were given the same project: germination studies In autumn 1989, we started writing a bookon seed dor- oncaryopsesofthetwosummerannualgrasses,Sporobolus mancyandgerminationfromanecological,biogeographical vaginiflorusandAristidalongespica. andevolutionaryperspective.Tooursurprise,wediscovered The plant autecology course gave us an awareness that many articles that had been published on these aspects of the general ecological question: Why do plants grow of seed biology were not in our files; thus, much time has where they do? Further, it was clear that a knowledge of beendevotedtoobtainingcopiesofthem.Aswewrotethis seed dormancy and germination requirements could be an book, new papers were appearing in the literature almost important part of the answer to this question. We were continuously,andattimesithasfeltlikewewereonafast- intriguedbystudiesonseedsofdesertplantsbyF.W.Went paced treadmill, i.e., new information was being published in southwestern USA and by M. Evenari, D. Koller and faster than it could be incorporated into the manuscript. others in Israel. Equally interesting were the results from However, the quantity and quality of new material being studies by B. Quinlivan on legume seeds in Australia and published on seed dormancy and germination is very excit- those of D. Ratcliffe and of E. Newman on winter annuals ing,andittestifiestotheinterestinthissubjectofscientists in England. In all these studies, seed and environmental allovertheworld. factors interacted to control the timing of germination in Work has been cited only if we have examined a copy nature. ofit.Itshouldbemadeclear,however,thatnoteverypubli- Our excitement about seeds was stimulated further cation on seed germination ecology has been (could be) by Dr. Lela V.Barton who came to VanderbiltUniversity included in this book. Some omissions are due to our for a visit. She patiently answered questions and told ignorance, and for that we apologize in advance to the us fascinating things about seeds, such as the different authorsand hopetheywillsenduscopiesof(orreferences dormancy-breaking/germination requirements of ray and to)theirwork. Otherstudiesmaynothavebeenmentioned disk achenes in some Asteraceae and double dormancy in because (1) they were very similar to representative ones seeds of Trillium. A tremendous stimulus to our interest alreadycited,or(2)themethodswerenotclearlystatedand inthedifferentkinds ofseeddormancyandhowthese are thusthemeaningoftheresultswasunclear.Wewouldlike broken in nature was provided by the publication of the tothankthelibrariansattheUniversityofKentuckyforall English translation of Dr. M. G. Nikolaeva’s (1967) book their help in finding and/or obtaining copies of references. PhysiologyofDeepDormancyinSeedsin1969. Special thanks are due to Bradley O. Grissom, Biology Overtheyears,ithasbeenourpleasuretostudytheseed Librarian, and to various people in the Interlibrary Loan germination ecology of numerous species. We have con- Department. centrated on herbaceous species but occasionally have We hope that this book will (1) provide people who investigated shrubs. These studies have included nonnative are just beginning to learn about seed germination a com- (weeds) and native geographically widespread, as well as prehensive overview of seed germination ecology, bioge- narrowly restricted (endemic), species. Most seeds have ography and evolution, and (2) give active researchers in comefromeasternUSA,andtheyhavebeencollectedfrom the field a sense of whatwe know and do not know about plants growing in arable fields, lawns, pastures, roadsides, these aspects of seed biology, and thus what research forests, prairies, rock outcrops and mudflats and other needstobedoneontheminthefuture. xiii Chapter 1 Introduction PURPOSE From a careful reading of Evenari’s (1980/81) paper on the history of germination research, one comes to the Each chapter in this book begins with a brief summary of conclusion that Theophrastus (c. 372(cid:1)287 B.C.) should be its purpose(s); thus, in keeping with this format, one called the Father of Seed Germination Ecology. This objective ofChapter1 istoexplain thephilosophy for the remarkableearlyGreekphilosopherandscientistknewthat: whole book. The original concept for this book was to (1)foodreservesare storedinseeds,(2)the environmental synthesize available information related to seed germina- conditions under which seeds mature affect their germina- tion ecology, including evolutionary aspects. However, as tion characteristics and (3) germination can be influenced the mass of information we were collecting on seed dor- byclimaticfactors,inhibitors,seedageandseedcoats. mancy and germination continued to increase, it became Determining what controls the timing of seed germi- clear that we should use this database to (1) determine if nation in the field requires information on the seed, plants with specialized life cycle and/or habitats were environmental conditions in the habitat and how the two unique with regard to seed dormancy and germination interact from time of seed maturation to germination. The characteristics, (2) obtain an understanding of the world best way to study the seed germination ecology of a biogeography of whole-seed dormancy and (3) formulate species is to break the problem into a series of questions: hypotheses concerning the origin and evolutionary rela- (1) When do seeds mature? (2) When are they dispersed? tionships of the various kinds of dormancy in seeds. (3) What is the natural germination unit, i.e., seed, fruit Thus, this book attempts to cover the present state of or fruit with accessory parts? (4) What is the dormancy knowledge of the ecology, biogeography and evolution state of seeds at the time of maturation and at dispersal? ofseeddormancyandgermination. (5) What are the environmental conditions in the habitat Other objectives of this introductory chapter are to between time of maturation and germination? (6) What explain what we mean by seed germination ecology, environmental conditions are required to break dormancy provide an overview of the general kinds of information and to induce it? (7) What conditions are required to needed to understand the seed germination ecology of a promotegerminationofnondormantseeds? species and comment on the values of such studies. Also, In the study of seed germination ecology, other kinds attention will be given to reasons why this book on seed of questions come tomind. For example, how do genetics germination is needed, and how it differs from previous and/or the climate under which seeds develop influence oneswrittenonthesubject. the requirements for dormancy break and germination? How much variation is there within a species? Does the SEED GERMINATION ECOLOGY species form a long-lived seed bank? Do buried seeds undergo changes in their dormancy state? What role does Much information is available in the literature on the seed timingofgerminationplayinaplant’sfitness? germinationphenologyofindividualspecies,andthesedata Since the days of Theophrastus, a vast amount of show that many species have a characteristic germination information related to seed germination has accumulated; season (or seasons). For many species, the time of year however, as can be seen in subsequent chapters, much when germination is possible is quite limited, e.g., only remains to be learned about some aspects of the field. inautumn,springorthewetseason.Incontrast,thegermi- There are two primary reasons why people are interested nation seasonfor other species is long, e.g., throughoutthe in learning how the timing of seed germination is con- growing season or even throughout the whole year. Thus, trolled under natural conditions: economics and aca- the broad objective of a seed germination ecologist is to demics. These two reasons for doing seed research are explain how the timing of germination is controlled in notindependent,anddiscoveriesbypeoplewithonepoint nature, and the ecological and evolutionary origins and of view frequently benefit those approaching the subject consequencesofthistiming. fromtheotherway. C.C.BaskinandJ.M.Baskin:Seeds,SecondEdition.DOI:http://dx.doi.org/10.1016/B978-0-12-416677-6.00001-9 ©2014ElsevierInc.Allrightsreserved. 1 2 Seeds Information on seed germination potentially has great Some books on seeds emphasize (1) chemical composi- monetary value. A knowledge of what controls the timing tion, physiology and biochemistry (Khan, 1977, 1982; ofgermination enhances(1) planning for effective control Bewley and Black, 1982, 1983, 1994; Labouriau, 1983; of weeds, (2) propagation of native economically impor- Murray, 1984; Zhang, 2004; Black et al., 2006; Bewley tant trees, shrubs, vines, forbs and grasses and (3) recla- etal.,2012),(2)typesofdormancy,andhowtheyarebroken mation of damaged ecosystems. Thus, much has been (Nikolaeva, 1969; Bradbeer, 1988), (3) structure (Corner, learned about seed germination from the research efforts 1976), (4) morphology (Davis, 1993) and (5) seed technol- of agronomists, foresters, rangeland specialists, reclama- ogy (Copeland and McDonald, 2001; Basra, 2006). Others tionecologistsandweedscientists. cover various aspects of seed physiology and/or dormancy Information on seed germination also is important and how environmental factors affect germination (Crocker because it contributes to a better understanding of certain and Barton, 1957; Heydecker, 1972; Kozlowski, 1972; biological concepts such as plant reproductive strategies, Fenner,1985;MayerandPoljakoff-Mayber,1989;Kigeland life history traits, adaptation to habitats and physiological Galili, 1995; Benech-Arnold and Sanchez, 2004). Books and molecular processes. Considerable research attention have been written (or compiled) on special topics such as hasbeengiventoseeddevelopmentandmaturation,storage embryo and seed development and germination and mobilization of food reserves, seed storage behavior— (Obroucheva, 1999; Batygina, 2006); seed aging (Priestley, especially of economicallyimportantplants, aging, cellular, 1986); identification (Bouman et al., 2000; Lentz and biochemical molecularevents in germinationand responses Dickau, 2005; Sweedman and Merritt, 2006); conservation of nondormantseeds to variousenvironmental factors,such (Smith et al., 2003; Guerrant et al., 2004); ecology (Fenner as temperature, light, soil moisture, nutrients and salinity. and Thompson, 2005); storage and longevity (Roberts, Thus, much has been (and continues to be) learned about 1972a;Sacandeetal.,2004);testing(Eliasetal.,2012);soil seedgerminationfromtheresearchofplantanatomists,bio- seedbanks(Lecketal.,1989;Thompsonetal.1997);germi- chemists,ecologists,geneticists,physiologistsandmolecular nationofdesertplants(Gutterman,1993,2002),flowerseeds biologists. (McDonaldandKwong,2005)andgrasses(Simpson,1990); restoration (Munoz et al., 1999; Elliott et al., 2005; L’Huillieretal.,2010);androleoftheseedsinregeneration A BOOK ON SEED DORMANCY AND ofplantcommunities(Fenner,1992a,2000).Itisnotuncom- GERMINATION FROM A DIFFERENT monforbookstocontainoneormorechaptersonthegermi- nation of special groups of plants such as orchids (Arditti, PERSPECTIVE 1977a, 1982; Rasmussen, 1995), grasses (Cheplick, 1998), Need halophytes (Ungar, 1991b), parasites (Parker and Riches, 1993), trees (Farmer, 1997), weeds (Benech-Arnold and Since information on seed germination is derived from Sanchez, 1995) or plants subjected to flooding (Scarano the research efforts of people in a wide variety of disci- and Franco,1998).A numberofhandbookshave been pub- plines, it should not be surprising that the data are pub- lishedthatprovidedetailedinstructionsonhowtogerminate lished in many different kinds of journals, in countries seedsofweeds(Andersen,1968),woodyplants(Youngand all over the world and in a variety of languages. Thus, Young, 1992; Compilation Committee, 2000; Schmidt, the general subject matter of journals that publish papers 2000; Vozzo, 2002; Piotto and Di Noi, 2003; Bonner and dealing with some aspect of seed germination ranges Karrfalt, 2008), native plants (e.g., Langkamp, 1987; from weed science, agronomy, crop science, range CullineyandKoebele,1999;Cullina,2000,2002b;Lilleeng- management, horticulture, forestry, botany, ecology, Rosenberger, 2005) and plants of interest to gardeners conservation biology, morphology, genetics, physiology, (Deno,1994). biochemistry and molecular biology. However, a few Although much information obviously was available journals, e.g., Journal of Seed Technology, Seed Science on seed germination ecology, it was scattered throughout and Technology, Seed Science Research, Journal of New the scientific literature. Thus, since no single comprehen- Seeds, Journal of Seed Research and Revista Brasileira sivesourceofdatawasavailableonthesubject,weunder- de Sementes, are devoted exclusively to seed research. took the task of doing a synthesis and published the first Information on seed germination also is found in agricul- edition of our seed book in 1998, which was issued in ture research station bulletins, dissertations and theses, paperback in 2001. As we continued to learn about seeds proceedings of symposia and conferences (e.g., Nicolas after July 1998, it quickly became clear that our “synthe- et al., 2003; Adkins et al., 2007), as well as in reviews sis” had not been totally successful—i.e., there was still a (e.g.,AnnualReviewofEcologyEvolutionandSystematics, lot more information that needed to be added to the book. Annual Review of Plant Physiology and Encyclopedia of Thus,wehavetriedtomeetthechallengebyaddinglarge PlantPhysiology)andinbooks. quantitiesofnewinformationtoSeeds. Chapter | 1 Introduction 3 A comprehensive synthesis of seed ecology will: synthesized for species with specialized life cycles and/or (1) facilitate and help focus research efforts, (2) identify habitats, including parasites, saprophytes, orchids, carnivo- questionsthatneedtobeaddressedbyadditionalresearch, rous plants, aquatics, halophytes and psammophytes, and (3)makeitpossibletoanalyzethepresenceofthevarious this information has been put into an ecological context; kinds of dormancy in different life forms of plants (i.e., (7) For the first time, an attempt has been made tounravel trees, shrubs, lianas and herbaceous species) in the major the evolutionary/phylogenetic origins and relationships of vegetationtypesoftheworldand(4)provideafoundation the various kinds of seed dormancy and to explain the towhichotherkinds ofinformation (such asfossil history conditionsunderwhicheachmayhaveevolved. and phylogenetic positions of families) can be added to The revision of our book has led to the expansion of formulatehypothesesontheevolutionofthevariouskinds many topics such as the definition of seed dormancy, ofseeddormancy. abscisic acid (ABA) and development of seed dormancy, phytochromes, hydrothermal time models, inbreeding Content depression and germination, animal predation of seeds, the two-step requirement for breaking physical dormancy, Our book differs from others on seed germination in watergapsinseedswithphysicaldormancyandhowthey seven important ways: (1) It contains a chapter on function and germination ecology of tropical montane procedures for doing germination studies so that labora- species. The database for the world biogeography of tory and greenhouse results can be extrapolated to the seed dormancy has been expanded from 3580 to about field;(2)Theuseofahierarchicalsystemofclassification 13,600 species, and the Takhtajan phylogenetic scheme of seed dormancy is discussed, along with the benefit of for angiosperms has been replaced by APG III (Chase using Nikolaeva’s formula system for dormancy classifi- and Reveal, 2009). Finally, each chapter now contains cationasameansoffacilitating internationalcommunica- one to many new topics such as need to check seeds for tion about the kind of seed dormancy being investigated; presenceofembryo;newplantcomesfromanundifferen- (3) Information on many topics—e.g., dormancy-breaking tiated embryo that develops into a differentiated embryo; requirements of seeds with each class of dormancy and dichotomous key for dormancy classes;physiological epi- genetics of seed dormancy and germination—is placed cotyldormancy;orchidseedfoodreservesandasymbiotic into an ecological context; (4) A critical evaluation of germination; nondeep simple epicotyl morphophysiologi- methodology used in soil seed bank studies of plant com- cal dormancy; sensitivity cycling in seeds with physical munities is presented, and it shows that many researchers dormancy; spatial distribution of seeds in the soil seed have sampled mixtures of persistent and transient seed bank and role of seed banks in restoration of plant com- banks rather than persistent seed banks only; (5) Data munities; testing dormancy evolution hypotheses; seed were compiled on species with different life forms grow- germination in relation to parental effects, pollen compe- ing in the major vegetation types worldwide to gain a tition, local adaptation, climate change, partial predation global perspective on geographical/ecological relationships of the seeds (and they still germinate), biological crusts, ofthedormancy-breaking and germinationrequirementsof nurse plants and karrikinolide in smoke from burning seeds; (6) Data on environmental conditions required to plants; and seed germination of rare and of invasive break seed dormancy and stimulate germination have been species.