The Necessity for Testing Germination of Fresh Seeds in Studies on Diaspore Heteromorphism As a Life-History Strategy

Seed Science Research (2013) 23, 83–88 doi:10.1017/S096025851300010X q Cambridge University Press 2013

RESEARCH OPINION

The necessity for testing germination of fresh seeds in studies on diaspore heteromorphism as a life-history strategy

Jerry M. Baskin1,2, Juan J. Lu1, Carol C. Baskin1,2,3* and Dun Y. Tan1 1Xinjiang Key Laboratory of Grassland Resources and Ecology and Ministry of Education Key Laboratory for Western Arid Region Grassland Resources and Ecology, College of Grassland and Environment Sciences, Xinjiang Agricultural University, Uru¨mqi 830052, China; 2Department of Biology, University of Kentucky, Lexington, KY 40506, USA; 3Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA

(Received 15 September 2012; accepted after revision 8 March 2013)

Abstract Introduction and background

Many studies have compared diaspore dispersal Diaspore heteromorphism is the production of two or ability and degree of dormancy in the two diaspores more seeds and/or fruits (sometimes with accessory of dimorphic plant species. A primary goal of these parts) on an individual plant that differ in many ways, studies was to determine if germination and dispersal such as morphology, mass, dispersal ability and characteristics of the two morphs fit within a high risk– degree of dormancy (Manda´k, 1997; Imbert, 2002). low risk (bet-hedging) life-history strategy, i.e. high There are two main categories of diaspore-hetero- dispersal/low dormancy in one morph versus low morphic plants: heterodiasporous and amphicarpous. dispersal/high dormancy in the other one. In a survey In heterodiaspory, two or more diaspore morphs are of 26 papers on 28 diaspore dimorphic species, we produced above ground, while in amphicarpy one or found that in 12 of the studies, which were published more diaspore morph(s) is (are) produced above between 1978 and 2008, seeds were stored, and thus ground and one or more below ground (Manda´k, 1997; possibly afterripened, before they were tested for Barker, 2005). Imbert (2002) listed 218 species that germination. The 14 papers that tested fresh seeds produce heteromorphic diaspores, and Wang et al. were published between 1963 and 2010. Failure to test (2010) reported that this phenomenon occurs in fresh seeds likely resulted in misinterpretation of the 26 families, 129 genera and 292 species of angiosperms. diaspore dispersal/dormancy strategy in some of the Depending on the species, the diaspores of hetero- species investigated. We conclude that it is imperative morphic species may be dimorphic (two morphs), that fresh seeds be tested for germination in order to trimorphic (three morphs) or polymorphic (more than be certain that the correct relationship between three morphs). However, the majority of hetero- dispersal and dormancy is elucidated, and thus that morphic species are heterodiasporous and produce the correct interpretation is made concerning life- two diaspore morphs (Imbert, 2002), and thus our history strategy and bet-hedging, in dimorphic survey was restricted to this group of plants. species. Diaspore dimorphism results in differences in dispersal, germination and post-germination beha- Keywords: afterripening, bet-hedging, diaspore dispersal, viour of the two morphs and is considered to be a bet-hedging strategy (Venable and Lawlor, 1980; dimorphic plants, fresh seeds, high risk–low risk heteromorphism, seed dormancy, stored seeds Venable, 1985; Ellner, 1986). For dispersal and dormancy, the usual result in studies on dimorphic species is that one diaspore has high dispersal ability and low (or no) seed dormancy and the other one low (or no) dispersal ability and high (or relatively high) *Correspondence seed dormancy (e.g. Venable and Lawlor, 1980; Ellner, Fax: 1-859-257-1717 1986). Diaspore heteromorphism for germination has Email: [email protected] been called high risk–low risk (HRLR) when the same 84 J.M. Baskin et al. factor (e.g. temperature) is more restrictive for stored diaspores were tested for germination. Using germination of one morph than the other, and high- these criteria, we selected 26 papers on diaspore risk–high-risk (HRHR) when different factors (e.g. light dimorphism, which included 28 species, to analyse in and temperature) are restrictive for germination of the our evaluation. The authors reported that diaspores two morphs (Venable, 1985; Venable et al., 1987). were stored in 12 (46%) of the studies, which were However, we suggest that it is impractical to use the published between 1978 and 2008, before the seeds same factor (HRLR) versus different factors (HRHR) were tested for germination. Fresh seeds were tested in for restricting germination to distinguish between the 14 of the studies, which were published between 1963 dormancy behaviour of the two heteromorphisms. As and 2010 (Table 1). A perusal of papers on fruit/seed Venable (1985) pointed out, germination of the two heteromorphism published more recently than those morphs would need to be compared in a variety of referenced in Table 1 shows that the practice of not laboratory or field environments to identify the testing fresh seeds is being continued (e.g. Atia et al., restrictive conditions for germination. Thus, it would 2011; Souza Filho and Takaki, 2011), as is the practice of seem that degree of dormancy, which integrates the testing fresh seeds in such studies (Cao et al., 2012; factors and their intensities affecting germination, is a Wang et al., 2012). more suitable way to compare restriction of germina- Diaspore dispersal ability and seed germination tion of the two morphs. In this paper, we consider only in 22 of the 28 species conformed to the H/H-L/L the dispersal and dormancy components of diaspore strategy, whereas in six they did not (Table 1). In heteromorphism and use ‘dormancy’ to include both three of the six species in which results deviated intensity and kind of restrictive factors for from the H/H-L/L model, seeds were stored before germination. they were tested for germination, and in the other Whereas Venable (1985) and Venable et al. (1987) three species seeds were not stored before testing. used a single letter (H) to designate high risk for all Fresh seeds were tested in 14 of the 22 cases that plant life-history traits, including dispersal and conformed to the H/H-L/L model and stored seeds dormancy, for one morph (i.e. HR) and a single letter in eight. (H or L) to designate high or low risk for these plant The kind of seed dormancy in the 28 species is life-history traits in the other morph (i.e. HR or LR), we non-deep physiological dormancy, and thus seeds use double-letters (or two different letters, see below) might be expected to have afterripened in dry to designate the diaspore dispersal ability and degree storage (Baskin and Baskin, 2004). We suggest that in of seed dormancy for a morph. Thus, for example, in the three of six species (seven cases, two for Crepis our scheme Venable’s HRLR is H/H-L/L. This double- sancta) in which seeds were stored and dispersal/ letter (or two-letter) designation seems necessary dormancy characteristics of two diaspores did not because not all morphs of dimorphic species have conform to the H/H-L/L model, the dormant morph either a high risk or a low risk combination of diaspore afterripened during storage, as illustrated in the dispersal ability and degree of seed dormancy; there much-cited study by Baker and O’Dowd (1982) on are ‘hybrid’ combinations (see below). achene-dimorphism in Hypochoeris glabra (Fig. 1) and Thus,tobecertainthatthedegreeofseed that the eight (of 22) species in which seeds were dormancy is identified correctly in the two morphs, stored but still conformed to the H/H-L/L model fresh seeds need to be tested for germination (‘dictum’ did not afterripen during storage. Of the three number 3 of Baskin et al., 2006). Lack of attention to the species that were not stored and still did not conform effect of storage on seed dormancy can cause to the H/H-L/L model, two of them [Grindelia misinterpretation of the relationship between diaspore squarrosa (McDonough, 1975) and G. lanceolata (Baskin heteromorphism and life-history strategy. Thus, the and Baskin, 1979)] lack a pappus on both disc (central) purpose of this opinion paper is to evaluate the and ray (peripheral) achenes and have little or no possible consequences of using stored seeds and not natural long-distance dispersal ability; thus, they do having data on germination of fresh seeds in drawing not (cannot) conform to the H/H-L/L model. Further, conclusions about dispersal ability and degree of fresh ray achenes of both species are more dormant dormancy in diaspores of dimorphic species. than fresh disc achenes, which is the usual case in Asteraceae. Thus, their dispersal/dormancy model is L/H-L/L. Results and discussion So, if we disregard the fact that both achene morphs of the two Grindelia species have low dispersal ability, For a paper to be included in our analysis, it had to then diaspores of only one of the three species, Atriplex contain information on: (1) dispersal ability that was tatarica, in which fresh diaspores were tested deviate measured or could be easily inferred from the from the H/H-L/L model. Thus, of the diaspores of description and/or illustrations of the two diaspore the six species that did not conform to the H/H-L/L morphs; (2) germination; and (3) whether fresh and/or model, three were stored and two did not have the The need to test fresh seeds 85

Table 1. Analysis of 26 studies on diaspore dispersal ability and degree of seed dormancy in the two diaspore morphs of 28 dimorphic species. In the column entitled ‘Dispersal/dormancy formula’, the ﬁrst two letters refer to one morph and the other two to the second morph. The ﬁrst letter of a pair of letters for a morph refers to diaspore dispersal ability and the second letter to degree of seed dormancy. H, high risk; L, low risk. In the ‘Storage’ column, ‘stored’ means seeds were stored before being tested for germination, but the authors did not say for how long. ‘Fresh’ means fresh seeds were tested

Dispersal/dormancy Species formula Storage Reference Amaranthaceae Aellenia autrani1 H/H-L/L Fresh Negbi and Tamari, 1963 Atriplex centralasiatica H/H-L/L Stored Li et al., 2008 A. tatarica H/L-H/H Fresh Manda´k, 2003 Salicornia patula H/H-L/L Stored Berger, 1985 Salsola komarovii H/H-L/L Fresh Yamaguchi et al., 1990 Suaeda aralocaspica H/H-L/L Fresh Wang et al., 2008 Asteraceae Bidens frondosa H/L-L/H 12 weeks Brandel, 2004 B. pilosa H/H-L/L Fresh Rocha, 1996 Carduus pycnocephalus H/H-L/L Fresh Olivieri et al., 1983 C. tenuiﬂorus H/H-L/L Fresh Olivieri et al., 1983 Crepis aspera H/H-L/L Fresh El-Keblawy, 2003 C. sancta H/H-L/H 8 months Imbert et al., 1996 C. sancta H/H-L/H 5–6 months Imbert, 1999 Grindelia lanceolata L/H-L/L Fresh Baskin and Baskin, 1979 G. squarrosa L/H-L/L Fresh McDonough, 1975 Hedypnois cretica H/H-L/L Fresh El-Keblawy, 2003 H. rhagadioloides H/H-L/L 6 months Kigel, 1992 Hemizonia increscens H/H-L/L Fresh Tanowitz et al., 1987 Heterotheca grandiﬂora H/H-L/L 5 months Flint and Palmblad, 1978 H. subaxillaris subsp. latifolia H/H-L/L Fresh Venable and Levin, 1985 H. subaxillaris subsp. subaxillaris H/H-L/L Fresh Baskin and Baskin, 1976 Hypochoeris glabra H/H-L/H 4–15 months Baker and O’Dowd, 1982 Leontodon longirrostris H/H-L/L c. 6–10 months Ruiz de Clavijo, 2001 L. saxatilis H/H-L/L 3–10 months Brandel, 2007 Senecio jacobaea H/H-L/L 4–5 months McEvoy, 1984 Boraginaceae Lappula duplicarpa H/H-L/L Fresh Ma et al., 2010 L. semiglabrata H/H-L/L Fresh Ma et al., 2010 Brassicaceae Diptychocarpus strictus H/H-L/L Fresh Lu et al., 2010 Fumariaceae Ceratocapnos heterocarpa H/H-L/L c. 6–10 months Ruiz de Clavijo, 1994

1 Information on this species also obtained from Werker and Many (1974). morphology (lack pappus, wings, etc.) that makes it second morph (L ! H). Interestingly, although possible for them to ﬁt the model; Atriplex tatarica is the achenes of C. sancta were stored for 8 months at only fresh-diaspore deviant. laboratory temperatures before they were tested for It seems likely that storage could have caused germination, Imbert et al. (1996) stated that neither changes in the dormancy state (via afterripening) of central nor peripheral achenes showed any dormancy morphs of the deviants, Bidens frondosa, Crepis sancta and that ‘... C. sancta is a high-risk strategy type’, and Hypochoeris glabra (Table 1). The dispersal/ apparently meaning HRHR (sensu Venable, 1985), since dormancy formula for C. sancta and H. glabra is neither of the two diaspore morphs were dormant. H/H-L/H, which could have been derived from However, if the fresh peripheral achenes were dormant, H/H-L/L via afterripening of the second morph as often is the case in Asteraceae, and they afterripened (i.e. L ! H) during storage. In B. frondosa, the formula during the 8-month storage period, then at fresh seed in H/L-L/H, which could have been derived from maturity the species would have had the high risk–low H/H-L/L during storage via the ﬁrst morph becoming risk (Venable’s HRLR) strategy. This proposed scenario more dormant (H ! L) and by afterripening in the is exactly like the one for H. glabra (Fig. 1). 86 J.M. Baskin et al.

Beaked CA (HDi) - Unbeaked PA (LDi)

If fresh PA seeds are more dormant If PA seeds stored for 4–15 mo (HDo) than CA, as they often are in (afterripened) before they were achene-dimorphic Asteraceae tested for germintion

Beaked CA (HDi/LDo) - PA (HDo→LDo) Beaked CA (HDi/LDo) - Unbeaked PA (LDi/HDo) Unbeaked PA (LDi/LDo)

Dormancy of PA (L→H)

High risk-Low risk H/H-L/H (this study) (H/H-L/L) HRHR (Venable, 1985)

Figure 1. An illustration of how the diaspore dispersal/dormancy relationship in Hypochoeris glabra (Baker and O’Dowd, 1982) may be misinterpreted, since fresh seeds were not tested for germination. CA, central achenes; PA, peripheral achenes; HDi, high diaspore dispersal ability; LDi, low (or no) diaspore dispersal ability; HDo, high (or relatively high) degree of seed dormancy; LDo, low (or no) degree of seed dormancy. Venable (1985) classiﬁed heteromorphism in H. glabra as high risk–high risk (his HRHR) since beaked achenes of this species are more light sensitive and non-beaked achenes more temperature sensitive. However, according to our scheme PA (L/H) is a mixture of low risk for diaspore dispersal (L) and high risk for seed dormancy (H).

Regarding the eight species that conformed to the from Israel that had been stored for 4–6 months at H/H-L/L model even after storage, there are three room temperature. In all 13 species, marginal possibilities to consider. First, fresh diaspores had a (peripheral) achenes were near-dispersed and central high risk–low risk strategy, and there was no change achenes far-dispersed, and the two morphs of in the dormancy status of either morph during storage. 10 species differed significantly in percentage and/or Second, dormancy in the H/H morph of stored seeds rate (speed) of germination. Thus, it reasonably can be could have been derived from H/L (i.e. L ! H) during concluded that the dispersal/dormancy characteristics storage; in which case, the dispersal/dormancy of fresh diaspores of 10 of the 13 species conform to formula of fresh seeds would have been H/L-L/L. the H/H-L/L model. However, without data on That is, seed dormancy in the first morph changed germination of fresh seeds one cannot be sure that the from low risk to high risk during storage via diaspores are assigned to the correct dormancy category afterripening. A third, more remote, possibility is at fresh maturity, i.e. low (or no) degree of dormancy that the (second) L/L morph in stored seeds is a versus a higher degree of non-deep physiological deviant of an L/H morph via stored seeds becoming dormancy. more dormant than fresh seeds during storage. Three of the species in Ellner’s study, Crepis aspera, Venable and Lawlor (1980) compiled information C. sancta and Hedypnois rhagadioloides, are present in from three major review-type sources on dispersal/ our survey. The dispersal/dormancy formula for fresh dormancy strategies of diaspores of 21 species of seeds of C. aspera in our study is H/H-L/L (Table 1), Asteraceae and six species of Brassicaceae. Eighteen whereas forstoredseeds inEllner’sstudy itis H/H-L/H, species of Asteraceae and five species of Brassicaceae which suggests thatperipheral(L/L)seedsafterripened conformed to the H/H-L/L model, whereas three and (i.e. L ! H) during dry storage. Indirectly, then, a one, respectively, did not. No information was given comparison of these two studies on the same species is by Venable and Lawlor (1980) about whether or not ‘proof’ that the dormancy status of a morph may change seeds of these 27 species were stored before they were during storage via afterripening. These results empha- tested for germination. Ellner (1986) tested germina- size the need to test germination of fresh diaspores to tion of 13 ligulate heteromorphic species of Asteraceae correctly interpret the tradeoffs between dormancy and The need to test fresh seeds 87 dispersal in fruit/seed dimorphic species. Our specu- Barker, N.P. 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