BIOTROPICA A Tropical,For Gregariously-Semelparous Peer Review Bamboo has Only no Seed Dormancy Journal: Biotropica Manuscript ID: BITR-07-015.R1 Manuscript Type: Paper Date Submitted by the n/a Author: Complete List of Authors: Bellairs, Sean; Charles Darwin University, School of Science and Primary Industries Franklin, Donald; Charles Darwin University, School for Environmental Research Hogarth, Nicholas; Charles Darwin University, School for Environmental Research Bambusa arnhemica, seed biology, monsoonal northern Australia, Keywords: bet-hedging, caryopsis, germination, Northern Territory, reproductive biology Association for Tropical Biology and Conservation Page 1 of 20 BIOTROPICA Bellairs, Franklin, and Hogarth NO SEED DORMANCY IN A BAMBOO 1 2 3 4 5 6 7 8 9 10 11 12 13 14 For Peer Review Only 15 16 17 18 19 20 21 22 23 24 25 A Tropical, Gregariously-Semelparous Bamboo has no Seed Dormancy 26 27 28 29 Sean M. Bellairs1 30 31 32 School of Science, Charles Darwin University, Darwin Northern Territory 0909, 33 34 Australia. 35 36 37 38 39 and 40 41 Donald C. Franklin and Nicholas J. Hogarth 42 43 44 School for Environmental Research, Charles Darwin University, Darwin Northern 45 46 Territory 0909, Australia. 47 48 49 50 1 51 Corresponding author. e-mail: [email protected] 52 53 54 55 Received ______; revision accepted ______ . 56 57 58 59 60 Association for Tropical Biology and Conservation BIOTROPICA Page 2 of 20 1 2 3 ABSTRACT 4 5 6 7 8 Seed dormancy may be disadvantageous for gregariously semelparous plants because it 9 10 11 disrupts the high levels of reproductive synchrony necessary for success. Alternately, it 12 13 may provide a bet-hedging option for an otherwise "all eggs in the one basket" 14 For Peer Review Only 15 reproductive strategy. Rapid germination of seeds upon hydration has been demonstrated 16 17 18 for a range of tropical, semelparous bamboos, but the fate of seeds that failed to 19 20 germinate promptly has been inadequately investigated. We demonstrate prompt 21 22 germination of seeds upon hydration and the absence of a dormant seed bank in a long- 23 24 25 lived, gregariously-semelparous bamboo, Bambusa arnhemica, from monsoonal northern 26 27 Australia. However, we refute the suggestion that seed dormancy is necessarily 28 29 maladaptive in a gregariously-semelparous plant. Rather, caryopsis dormancy may not be 30 31 32 possible in a seasonally-moist tropical climate. Given an inability to adjust or bet-hedge 33 34 their germination, bamboo germinants must cope with the vagaries of the monsoonal 35 36 37 climate, a factor which may contribute to the general restriction of bamboos to regions 38 39 with higher rainfall. 40 41 42 43 44 45 46 Key words: Bambusa arnhemica; bet-hedging; caryopsis; germination; monsoonal 47 48 northern Australia; Northern Territory; reproductive biology; seed biology 49 50 51 52 53 54 55 56 57 58 59 60 2 Association for Tropical Biology and Conservation Page 3 of 20 BIOTROPICA 1 2 3 THE EXTRAORDINARY GREGARIOUS SEMELPARITY OF MANY LONG-LIVED BAMBOOS offers 4 5 6 few opportunities for bet-hedging against total reproductive failure. Not only do 7 8 individuals (genets) flower once and then die after decades or even centuries of clonal 9 10 11 growth (Janzen 1976), but neighbours who presumably include kin do so at the same 12 13 time. Furthermore, as flowering appears to be triggered by a biological clock that is 14 For Peer Review Only 15 impervious to immediate environmental conditions (Kawamura 1927, Franklin 2004), 16 17 18 there is no obvious process by which the bamboo may respond to variation among years 19 20 to ensure that suitable environmental conditions prevail at the time of sexual 21 22 reproduction. 23 24 25 26 27 Many plants hedge their reproductive "bets" through seed dormancy mechanisms 28 29 that stagger germination or delay it until suitable conditions prevail (Rees 1997). Seed 30 31 32 dormancy mechanisms are prevalent in semelparous annuals but surprisingly rare in long- 33 34 lived semelparous species (Young & Augspurger 1991). Numerous studies of tropical 35 36 37 bamboos report prompt and high germination rates upon hydration (often around 80%) 38 39 and/or marked declines in seed viability within a matter of months (White 1947, Mohan 40 41 Ram & Hari Gopal 1981, Wong 1981, Kondas 1982, Venkatesh 1984, Azmy 1994, Banik 42 43 44 1994, Ravikumar et al. 1998a,b, Koshy & Harikumar 2001, Rawat & Thapliyal 2003). 45 46 From these it has been inferred that semelparous bamboos lack seed dormancy 47 48 mechanisms (Janzen 1976). However, in a perusal of this literature we could find no 49 50 51 evidence concerning the fate of seeds that failed to germinate promptly, reflecting a 52 53 prevailing horticultural rather than ecological perspective. Seed dormancy has been 54 55 demonstrated or robustly inferred in several temperate-zone bamboos (Matumura & 56 57 58 59 60 3 Association for Tropical Biology and Conservation BIOTROPICA Page 4 of 20 1 2 3 Nakajima 1981, Taylor & Qin 1988). 4 5 6 7 8 Short-term dormancy of a proportion of seeds could be a successful bet-hedging 9 10 11 strategy in a tropical monsoonal climate (Andrew & Mott 1983) where the early storms 12 13 of the wet season are often followed by periods of intense heat and dryness before 14 For Peer Review Only 15 monsoonal rains set in (Cook & Heerdegen 2001). Longer-term dormancy – delaying 16 17 18 germination of some seeds for a year – might be a viable bet-hedge against the failure of 19 20 wet season rains or other reproductive catastrophes. However, Janzen (1976) argued that 21 22 inter-annual delays would be selected against in gregariously semelparous bamboos 23 24 25 because it would generate disadvantageous reproductive asynchrony in the subsequent 26 27 generation. 28 29 30 31 32 In this note, we examine the germination strategy of a gregariously semelparous 33 34 bamboo, Bambusa arnhemica. Bambusa arnhemica is a pachymorph (clumping) bamboo 35 36 37 endemic to the north-west of the Northern Territory of Australia (Franklin 2003). The 38 39 region has a monsoonal tropical climate with almost all rain falling between October and 40 41 April. Bambusa arnhemica occurs in areas with a mean annual rainfall of from 1200 to 42 43 44 1750 mm, mostly in riparian forests but occasionally on rocky hillsides (Franklin & 45 46 Bowman 2004). The species flowers gregariously at the end of a genet lifespan estimated 47 48 to be 40–50 yr (Franklin 2004). Flowering commences in the dry season and continues 49 50 51 until the early wet season. Production and drop of the c. 20 mg caryopses is concentrated 52 53 at about the time of the first storms of the wet season in October to December and 54 55 numerous seedlings appear promptly after substantial storms. Seed production is prolific 56 57 58 59 60 4 Association for Tropical Biology and Conservation Page 5 of 20 BIOTROPICA 1 2 3 such that the ground below seeding clumps may be carpeted with seeds (D. Franklin & N. 4 5 6 Hogarth, pers. obs.). 7 8 9 10 11 12 13 14 For Peer Review Only 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 5 Association for Tropical Biology and Conservation BIOTROPICA Page 6 of 20 1 2 3 METHODS 4 5 6 7 8 Seed and soil samples were collected from four locations in the 2005/06 wet season: Mt 9 10 11 Bundy Creek (MBC – 12°50’ S, 131°35' E), Annaburroo Station (AS – 12°53’ S, 131°42' 12 13 E) and two sites at the Mary River Wildlife Ranch (MR1 & MR2 – 1.0 km apart at 14 For Peer Review Only 15 13°36’ S, 132°13” E). MBC, MR1 and MR2 were on river banks, whereas the AS site 16 17 18 was a rocky hillside. For each site, seeds and associated dry florets (with or without 19 20 seeds) were collected from at least four B. arnhemica clumps in November 2005 and 21 22 pooled. Topsoil samples were collected in March 2006, replicate samples being collected 23 24 25 from within 1 m of the base of four B. arnhemica clumps that had seeded per site, each 26 27 sample containing twenty cores of 8 cm diameter by 5 cm depth. Seedlings were counted 28 29 in March 2006 within 1 m of the base of each of four clumps per site, each clump being 30 31 32 sampled with three 20 by 10 cm quadrats. At one site where the seedling density was very 33 34 low, quadrat size was increased to 1 by 1 m and placed within 2 m of the clump base. 35 36 37 38 39 Seeds and associated dry florets were dried in an air-conditioned room for two 40 41 weeks and then stored at 25°C in an airtight container with a silica bag to reduce 42 43 44 humidity until needed for viability and germination trials. Upon retrieval for viability and 45 46 germination trials, florets containing seeds were identified by their swollen firmness 47 48 compared to empty dry florets. After removal of the husks, four sub-samples of 50 seeds 49 50 51 per site were weighed on an electronic balance to 0.1 mg. 52 53 54 55 56 57 58 59 60 6 Association for Tropical Biology and Conservation Page 7 of 20 BIOTROPICA 1 2 3 Seed viability was assessed c.