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Effects of seed size and habitat on recruitment patterns in grassland and forest plants Karin Lönnberg ©Karin Lönnberg, Stockholm University 2012 ISBN 978-91-7447-599-9 Printed in Sweden by US-AB, Stockholm 2012 Distributor: Department of Botany, Stockholm University Till Ida och Gustav Doctoral dissertation Karin Lönnberg Department of Botany Stockholm University SE-106 91 Stockholm Sweden Effects of seed size and habitat on recruitment patterns Abstract – A trade-off between seed size and seed number is central in seed ecology, and has been suggested to be related to a trade-off between competition and colonization, as well as to a trade-off between stress tolerance and fecundity. Large seeds endure hazards during establishment, such as shading, drought, litter coverage and competition from other plants, better than do small seeds, due to a larger amount of stored resources in the seed. Small seeds, however, are numerous and small-seeded species are therefore more fecund. Moreover, a pattern with small-seeded species being associated with open habitats and large-seeded species being associated with closed habitats has been reported in the literature. In this thesis I assess effects of seed size on recruitment, and how relationships between seed size and recruitment may relate to habitat conditions. Seed sowing experiments were performed in the field to assess interand intra-specific relationships between seed size and recruitment in open and closed habitats (Paper I and II). Seed removal experiments were performed in the field to assess what effects seed predation may have on a relationship between seed size and recruitment (Paper III). A garden experiment was performed based on contests between larger-seeded and smaller-seeded species, in order to examine different models on coexistence of multiple seed size strategies. The results showed that there was a weak positive relationship between seed size and recruitment in the field, and that this relationship was only weakly and inconclusively related to habitat (Paper I and II). Seed removal was negatively related to seed size in closed habitats and unrelated to seed size in open habitats (Paper III). This indicates that any positive relationship between seed size and recruitment may be an effect of higher seed removal in small-seeded species. However, when grown under controlled conditions in a garden experiment, there was a clear advantage of larger-seeded species over smaller-seeded species (Paper IV). This advantage was unaffected by seed density, indicating that there was no competitive advantage of the larger-seeded species. Instead, indirect evidence suggests that largerseeded species exhibit higher tolerance to stress. Keywords – Seed size, seedling establishment, seedling survival, recruitment, seed removal, co-existence, game-theory List of papers This thesis is based on the following papers, which are referred to by their roman numerals: I. Lönnberg K, Eriksson O (2012) Seed size and recruitment patterns in a gradient from grassland to forest. Ecoscience 19: 140-147. II. Lönnberg K, Eriksson O. Relationships between intra-specific variation in seed size and recruitment in four species in two contrasting habitats. Plant Biology, doi: 10.1111/j.14388677.2012.00676.x III. Lönnberg K. Seed removal in relation to seed size in two contrasting habitats. Manuscript. IV. Lönnberg K, Eriksson O. Rules of the seed size game: contests between large-seeded and small-seeded species. Accepted for publication in Oikos, doi: 10.1111/j.16000706.2012.00246.x Contents Introduction ....................................................................................................... 11 Background .................................................................................................... 11 Co-existence of multiple seed sizes ............................................................... 12 Study system and study area ......................................................................... 14 Aim..................................................................................................................... 15 Methods ............................................................................................................ 15 Results and discussion ....................................................................................... 17 Concluding remarks ........................................................................................... 21 Acknowledgements ........................................................................................... 21 References ......................................................................................................... 21 Svensk sammanfattning .................................................................................... 26 Tack! .................................................................................................................. 31 10 Introduction Background Parents invest a lot of resources in their offspring. In plants, the seed is an important part of the plant life cycle, and seed size has been shown to affect, for example, seed predation (Gómez 2004; Pérez-Ramos et al. 2008; Gómez et al. 2008), longevity in soil (Thompson et al. 1993; Moles et al. 2000), germination (Gómez 2004; Moles & Westoby 2004a; Urbieta et al. 2008) and seedling survival (Paz & Martínez-Ramos 2003; Moles & Westoby 2004b; Baraloto et al. 2005). Among plants there is a huge variation in seed size stretching over ten orders of magnitude, from the dust-like seeds of orchids and some saprophytic and parasitic plants weighing about 1µg, to the double coconut weighing up to 20 kg (Harper et al. 1970). Furthermore, among plants within a plant community there is a variation in seed size typically stretching over five to six orders of magnitude (Leishman et al. 2000; Westoby et al. 2002). A central part of seed ecology is the trade-off between seed size and seed number, which is based on a model of an offspring size – number tradeoff (Smith & Fretwell 1974). This model states that from a given amount of resources allocated to seed production a plant can either produce a large number of small seeds, or a small number of large seeds. Large seeds are well provisioned for and have a high recruitment probability, whereas producing numerous (small) seeds enhances dispersal and gives a high fecundity. Seedlings germinating from large seeds are larger, and can endure hazards during establishment better than seedling germinating from small seeds, due to a larger amount of resources stored in the seed. For instance, large-seeded species have been shown to have a higher survival at the seedling stage than small-seeded species through events of drought, herbivory, litter coverage, shade and competition from established vegetation (Gross & Werner 1982; Gross 1984; Leishman et al. 2000; Westoby et al. 2002; Moles & Westoby 2004a). This would indicate that large seeds are advantageous in certain habitats, such as in stressful environments or in closed-canopy habitats with thick litter layers and where shading is massive. However, producing a few large seeds may involve costs for the plant. Producing a few large seeds, rather than 11 numerous small seeds, reduces fecundity and dispersability. Moreover, based on theory on optimal foraging, large seeds constitute a more desirable food source for seed predators, such as small rodents (Charnov 1976; Hoffmann et al. 1995; Hulme 1997; Blate et al. 1998; Hulme 1998). Large seeds are also more conspicuous, and take longer time to become incorporated into the soil, and therefore run a higher risk of being encountered by seed predators (Moles et al. 2003). Hence, producing large seeds would only be evolutionary stable under hazardous conditions, such as stressful or shady habitats, where the costs of having large seeds are balanced by the advantages (Leishman et al. 2000). In an open habitat, like a grassland, where there is less shading and competition from other plants is reduced through disturbance, the costs of having large seeds may not be balanced by the advantages (Eriksson & Jakobsson 1999). Producing numerous small seeds and thereby increasing fecundity and dispersability may instead be more advantageous, as producing numerous seeds increases the probability that at least some seeds find unoccupied and suitable microsites. Thus, species filtering and evolutionary processes favoring large-seeded species in closed and stressful habitats, and small-seeded species in open habitats are expected. Patterns with small-seeded species being associated with open habitats early in the succession sere, and large-seeded species being associated with closed, late succession habitats have indeed been found , and average seed size is generally higher in closed habitats than in open habitats (Baker 1972; Leishman et al. 2000; Bolmgren & Eriksson 2005). Co-existence of multiple seed sizes According to the model by Smith & Fretwell (1974), for each set of environmental conditions, there is an optimal seed size that is reached when offspring fitness is exactly balanced by energy invested per seed by the mother plant. This model states that any increase in seed size would increase offspring fitness, but this gain would not compensate the loss in fecundity, resulting in a total decrease in fitness for the mother plant. Any decrease in seed size would increase the fecundity of the mother plant, but would at the same time reduce offspring fitness, also resulting in a total decrease in mother plant fitness. Thus, any increase or decrease in seed size would be selected against. However, in nature seed sizes typically vary over five to six orders of magnitude among plants within 12 plant communities (Leishman et al. 2000; Westoby et al. 2002). Moreover, within plant species or even within plant individuals there is often a large variation in seed size (Obeso 1993; Vaughton & Ramsey 1998; Leishman et al. 2000), and little support for an optimal seed size has actually been found. This co-existence of multiple seed sizes has been puzzling, and density dependent game-theory has attempted to explain co-existence of multiple seed size strategies within plant communities. In this kind of models, developed by Geritz (1995) and Rees & Westoby (1997), asymmetric competition is assumed, such that larger seeds will always win over smaller seeds in direct competition over safe sites, leading to a competitive advantage in large seeds, but a colonization advantage in small seeds. Thus, large-seeded species can always invade any plant community, due to a competitive advantage. However, due to their higher abundance, small-seeded species can always invade any plant community because they will have the highest probability to be the first to find safe sites unoccupied by any larger seeds. For this model to work a complete asymmetry of competitive advantage is essential, such that even a minute difference in seed size would mean a complete advantage of the larger-seeded species, outcompeting the smaller-seeded species in every single case. Empirical studies, however, have found that the competitive advantage of largerseeded species is not completely asymmetric, and larger-seeded species do not always win over smaller-seeded species in direct competition over safe sites (Eriksson 2005). Moreover, in a study on seed size and species abundance, no relationship was found between seed size and abundance, indicating that small seeds are not generally more abundant than large seeds (Eriksson & Jakobsson 1998). Recently, a model by Muller-Landau (2010) has attempted to explain the co-existence of multiple seed size strategies, suggesting a seed-size game where the seed size – number trade-off is related to a trade-off between stress tolerance and fecundity, rather than a trade-off between competition and colonization. In this model large seeds are assumed to tolerate stress during establishment better than small seeds. Therefore, in stressful environments largerseeded species have an advantage over smaller-seeded species, whereas smaller-seeded species have an advantage in less stressful environments due to their higher fecundity. 13 Study system and study area In this thesis I have assessed seed size and habitat effects on recruitment patterns, working with a study system consisting of both a seed size gradient and a habitat gradient. As all experiments were conducted in south-eastern Sweden, plant species and habitats common in the area were used. The habitat gradient is a conceptual gradient stretching from an open disturbance regime to a closed competition regime. For the field experiments I selected a gradient from grassland to forest to represent this conceptual gradient, using both a gradient represented by six habitats from heavily grazed grassland to coniferous forest (Paper I), and two contrasting habitats – grassland and deciduous forest (Paper II and Paper III). For the garden experiment (Paper IV) different treatments of litter and shading were used to mimic conditions expected to have high influence on recruitment in open and closed habitats. The seed size gradient consisted of seeds of plant species selected to represent a variation in seed size among species (Paper I, III and IV) from small-seeded to large-seeded, as well as within species (Paper II). All selected plant species are common in the area, which was essential in order to make collections of large numbers of seeds possible. Some of the selected species mainly inhabit open habitats, whereas others are mainly found in closed habitats, although all selected species are habitat generalists, and occur in both open and closed habitats. Care was also taken to select species from different plant genera, and as far as possible also from different plant families, in order to avoid phylogenetically biased sampling. The field experiments were conducted in Tullgarn (Paper I and II) and Angarn (Paper III). The Tullgarn area is a nature reserve situated by the Baltic Sea, about 45 km southeast of Stockholm (WGS 84 lat, lon: 58.95045, 17.58410). The area has a long history of management and consists of a variety of habitats, from open and semi-open grasslands mainly grazed by cattle, to deciduous and coniferous forests. The Angarn area, too, is a nature reserve, about 25 km north of Stockholm (WGS 84 lat, lon: 59.54270, 18.14809). The reserve is dominated by a bird lake, surrounded by a mosaic of grassland grazed by cattle and horses, arable fields and mixed deciduous and coniferous forests. The garden experiment (Paper III) was conducted in a garden at the Department of Botany, Stockholm University. 14 Aim The objectives of this thesis were to assess relationships between seed size, recruitment and habitat. This was done by addressing the following questions: Is there a relationship between seed size and recruitment at the interspecific level (Paper I) and intra-specific level (Paper II)? If so, does this relationship shift as the habitat shifts from open to closed (Paper I+II)? Is there evidence for species filtering processes (Paper I) or selection (Paper II) favoring large-seeded species in closed habitats and small-seeded species in open habitats? Is there a relationship between seed size and seed predation, and what implications may that have in recruitment patterns (Paper III)? Do larger-seeded species generally win over smaller-seeded species in direct contest over safe sites, and does any seed size advantage increase in high competition or stressful conditions (Paper IV)? Methods To assess seed size effects on recruitment patterns in relation to different plant community conditions I have performed seed sowing experiments in the field (paper I + II) and in a common garden (paper IV), as well as a seed removal experiment in the field (paper III). Twenty-four plant species, from fifteen plant families, were initially selected for the two seed sowing experiments in the field (paper I + II). The plant species were selected because (i) they all occur in both open and closed habitats in the study area, (ii) there is a large variation in seed size among, and in some cases also within, the species, and (iii) all species are common in the study area which made collection of large numbers of seeds possible. Fourteen of the species were later also used in the common garden 15 experiment (paper IV) and ten of the species were used in the seed removal experiment (paper III). Paper I To study the effects of seed size and habitat on recruitment, I selected six vegetation types to represent a gradient from grassland to forest. Seeds of 20 plant species, with a 356-fold inter-specific variation in seed size, were sown in six sites of each vegetation type. Seed sowings were performed in two consecutive years, 2005 and 2006. Seedling emergence and seedling survival was recorded in the beginning and end of each growing season, for up to three years. Paper II To assess intra-specific relationships between seed size and recruitment in different habitats, I weighed seeds of four plant species (Convallaria majalis, Frangula alnus, Prunus padus and P. spinosa) individually, 3200 seeds per species. The seeds were sown one by one, while carefully keeping track of each single individual, in two contrasting habitats, grassland and deciduous forest. Seed sowings were performed in two consecutive years, 2005 and 2006. The fate of each individual seed, in terms of seedling emergence and seedling survival, was followed for up to three years. Paper III To assess whether seed predation may play a role in any relationships between seed size and recruitment, I conducted seed removal experiments where seed removal was used as a measure of seed predation. Seeds of ten plant species varying 1452-fold in seed size were placed one by one in field sites representing two contrasting habitats, grassland and deciduous forest. After 48 hours seed removal was recorded. The set up was repeated seven times in each of ten sites. 16 Paper IV To test whether larger-seeded species have an advantage over smallerseeded species in direct contests, and if such an advantage increases in conditions with shade and/or litter, I conducted a garden experiment where seeds of 14 plants species were sown pair-wise in pots. Each pair consisted of one larger-seeded and one smaller-seeded species. The seeds were grown in six different treatments of seed density, shade and litter, and seedling emergence and seedling survival for both species of all species pairs were followed for two years. Results and discussion In Paper I, I found that generally there was a weak positive relationship between seed size and recruitment among plant species, and that this relationship was only weakly affected by habitat. Seed sowings were performed in two consecutive years, and the recruitment differed between years. Among the six habitats selected to represent a gradient from open to closed habitat, there was no relationship between seed size and recruitment in the two most open grassland habitats, whereas positive relationships were found in the four most closed habitats, for seeds sown in 2005. For seeds sown in 2006 there was a positive relationship between seed size and recruitment only in one habitat – poorly grazed grassland, the second most open habitat, whereas no relationship was found for any of the other five habitats. In Paper II, I found that within species there were positive relationships between seed size and emergence, and between seed size and recruitment. Here, too, seedling emergence and final recruitment differed between years, indicating that seeds sown in 2006 met harsher conditions during establishment than seeds sown in 2005. Only weak effects of habitat were found; within one species (Convallaria majalis) final recruitment was positively related to seed size in the closed habitat, but not in the open habitat, whereas within another species (Prunus spinosa) final recruitment was positively related to seed size in the open habitat, but not in the closed habitat. Within the other two species (Frangula alnus and Prunus padus) any relationships 17 between seed size and recruitment were unrelated to habitat. The results from these two studies show a coherent pattern between inter-specific and intra-specific recruitment patterns in the study system. Both at the inter-specific and at the intra-specific level there was a positive effect of seed size on recruitment, and habitat effects on this relationship were weak. This indicates that factors other than those associated with habitats, such as variation in abiotic factors between years, may have a large effect on recruitment. A species filtering process, favoring smallseeded species in open habitats and large-seeded species in closed habitats is suggested, but that such a filter only is active during certain conditions (Paper I). No clear evidence of a selection pressure favoring small seeds in open habitats and large seeds in closed habitats was found, which suggests that opposing selection pressures may instead have a stabilizing effect on seed size (Paper II). From these two papers I suggest the following mechanism to explain recruitment patterns in a gradient from grassland to forest habitats: 1) When seeds are subjected to minor hazards during establishment, i.e. during favorable years and in open habitats, all seeds recruit equally well, resulting in seed size having no effect on recruitment. 2) When seeds are subjected to major hazards, i.e. during harsh years in closed habitats, all seeds recruit equally poorly and seed size, again, has no effect on recruitment. 3) When subjected to intermediate hazards during establishment, i.e. during favorable years in closed habitats, or during harsh years in open habitats, seed size has a positive effect on recruitment. This is consistent with the model by Muller-Landau (2010), suggesting that a wide range of seed sizes manage to recruit in low stress environments, whereas only large seeds manage to recruit in high stress environments. Seeds establishing in a grassland during a favorable year thus meet low stress conditions, resulting in all seed sizes recruiting equally well. In Paper I an equal number (50) of seeds were sown per plot, and therefore no difference in recruitment between seed sizes was found. At the other extreme, seeds establishing in a forest during a harsh year meet multiple hazards (e.g. shading, litter, competition and drought). In such multiple hazard conditions, the environment may be too stressful for successful recruitment to occur in any seed size, again resulting in no difference in recruitment between seed sizes. However, seeds establishing in a grassland during a harsh year, or in a forest during a favorable year meet intermediate stress conditions. In these conditions only seeds larger than a certain size manage to recruit, resulting in a 18 positive relationship between seed size and recruitment. To fully understand this recruitment pattern, further detailed studies to assess under which conditions seed size has a positive effect on recruitment, and under which conditions recruitment is unrelated to seed size are required. The results from Paper III showed that seed removal was much higher in closed habitats than in open habitats, in most species as much as twice as high. This was expected as closed habitats probably provide more safe sites for seed predators, and is consistent with results from previous studies (Mittlebach & Gross 1984; Reader 1991; Osunkoya 1994; Hau 1997). Based on the theory on optimal foraging I also expected to find a positive relationship between seed size and seed removal. Quite contrary, however, I found a negative effect of seed size on seed removal in closed habitat and no relationship in open habitat. Most previous studies have typically found a positive relationship between seed size and seed predation (Reader 1993; Hoffmann et al. 1995; Hulme 1998; Gómez 2004; Pérez-Ramos 2008), or that factors other than seed size control seed predation rates (Mittlebach & Gross 1984; Hau 1997; Holl & Lulow 1997; Meiners & Stiles 1997; Kollmann et al. 1998). A few studies have, in coherence with my study, found negative relationships between seed size and seed predation (Osunkoya 1994; Blate et al. 1998; Moles et al. 2003). In some cases a negative relationship is explained by that larger seeds have harder seeds coats, and therefore smaller seeds are preferred by seed predators (Osunkoya 1994). This explanation is unlikely in my study, as the largest seeds within this study were cherry kernels, known to be a desirable food source to small rodents (personal observation). My study assessed a rather wide range of seed sizes, from 0.14 mg – 203 mg. In a previous study where a similarly wide range of seed sizes were assessed, a negative relationship between seed size and seed removal was also found (Moles et al. 2003), and explained by different guilds of seed predators feeding on different seed sizes. This explanation seems likely in my study, given that different guilds of seed predators have different habits and abundance. Another explanation may be that smaller seeds are removed through secondary dispersal, rather than by seed predators. The results from Paper III may offer some explanation to the positive relationship between seed size and recruitment found in Paper I and II. If smaller seeds are removed at a higher rate than larger seeds, this may explain why recruitment is lower in smaller seeds. The result that there was no relationship between seed size and seed removal in open habitats 19 is coherent with results from Paper I, showing no relationship between seed size and recruitment in open habitats. If all seed sizes are removed at the same rate, all seed would be expected to have the same probability of recruitment, given that seed size is unrelated to recruitment. The result that there was a negative relationship between seed size and seed removal in closed habitat is also coherent with results from Paper I, showing a positive relationship between seed size and recruitment in closed habitats. If small seeds are removed at a higher rate, a lower probability of recruitment in small seeds would be expected, resulting in a positive relationship between seed size and recruitment, even if seed size was unrelated to recruitment. The results from Paper IV showed that larger-seeded species generally had an advantage over smaller-seeded species in direct contests for safe sites. This advantage increased in strength in treatments with litter, compared to when not subjected to litter, whereas shading and seed density had no effect on the strength of the advantage. My study provides no direct evidence as to whether this advantage of larger-seeded species is a result of higher competitive ability or tolerance to stress. However, indirect support for a model based on a trade-off between tolerance to stress and fecundity is given, as seed density had no effect on the strength of the advantage of the larger-seeded species, which would be expected in a competition – colonization driven mechanism. In Paper I and II only weak effects of seed size on recruitment was found, whereas in Paper IV a clear advantage of larger-seeded species was found. This incoherence may be resulted from confounding factors in the field obscuring any relationship between seed size and recruitment. In the garden experiment these confounding factors were eliminated, with a clearer signal as a result. In the field it is often difficult to isolate different factors from each other, and what effects they may have. The results from Paper IV indicate that negative effects on recruitment in closed habitats may be an effect of litter (among others), but that the effect of shading is minor. 20 Concluding remarks The general conclusions of this thesis are that seed size has a positive effect on recruitment. This positive effect is weak in field conditions, but stronger when confounding effects in the field are controlled for in a garden experiment. Habitat effects on the positive relationship between seed size and recruitment are weak and inconclusive, and only occur under certain conditions. Other factors, such as differences in abiotic factors between years, may have a higher influence on any relationship between seed size and recruitment. However, when isolated from confounding factors in the field, there is a clear effect of litter, increasing the advantage of larger-seeded species. Any positive relationship between seed size and recruitment may, however, be an effect of higher seed removal in small-seeded species within the study area. There is no evidence of a competitive advantage in larger-seeded species, but rather indirect evidence is found for a better ability to tolerate stress in largerseeded species. Acknowledgments I am grateful to Ove Eriksson, Kjell Bolmgren and Ellen Schagerström for valuable comments on this thesis. References Baker, H G (1972). Seed weight in relation to environmental conditions in California. Ecology 6: 997-1010. 21 Baraloto C, Forget P-M, Goldberg D E (2005). Seed mass, seedling size and neotropical tree seedling establishment. 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Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58: 71-80. Gómez J M, Puerta-Piñero C, Schupp E W (2008). Effectiveness of rodents as local seed dispersers of Holm oaks. Oecologia 155: 529-537. Gross K L, Werner P A (1982). Colonizing abilities of “biennial” plant species in relation to ground cover: implications for their distributions in a successional sere. Ecology 63: 921-931. Gross K L (1984). Effects of seed size and growth form on seedling establishment of siz monocarpic perennial plants. Journal of Ecology 72: 369-387. 22 Harper J L, Lovell P H, Moore K G (1970). The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1: 327356. Hau C H (1997). Tree seed predation on degraded hillsides in Hong Kong. Forest Ecology and Management 99: 215-221. Hoffmann L A, Redente E F, McEwen L C (1995). Effects of selective seed predation by rodents on shortgrass establishment. Ecological Applications 5: 200-208. 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Journal of the Torrey Botanical Society 124: 67-70. Mittelbach G G, Gross K L (1984) Experimental studies of seed predation in old-fields. Oecologia 65: 7-13. 23 Moles, A. T. Hodson D W, Webb C J (2000). Seed size and shape and persistence in the soil in the New Zealand flora. Oikos 89: 541-545. Moles A T, Warton D I, Westoby M (2003). Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84: 3148-3161. Moles A T, Westoby M (2004a). Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92: 372-383. Moles A T, Westoby M (2004b). What do seedlings die from and what are the implications for evolution of seed size? Oikos 106: 193199. Muller-Landau H C (2010). The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proceedings of the National Academy of Sciences. Obeso J R (1993). Seed mass variation in the perennial herb Asphodelus albus: sources of variation and position effect. Oecologia 93: 571-575. Osunkoya O O (1994). Postdispersal survivorship of north Queensland rainforest seeds and fruits: Effects of forest, habitat and species. Australian Journal of Ecology 19: 52-64. Paz H, Martínez-Ramos M (2003). Seed mass and seedling performance within eight species of Psychotria (Rubiaceae). Ecology 84: 439-450. Pérez-Ramos I M, Urbieta I R, Marañón T, Zavala M A, Kobe R K (2008). Seed removal in two coexisitng oak species: ecological consequences of seed size. Plant cover and seeddrop timing. Oikos 117: 1386-1396. Reader R J (1991). Control of seedling emergence by ground cover: a potential mechanism involving seed predation. Canadian Journal of Botany 69: 2084-2087. 24 Reader R J (1993). Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. Journal of Ecology 81: 169-175. Rees M, Westoby M (1997). Game-theoretical evolution of seed mass in multi-species ecological models. Oikos 78: 116-126. Smith C C, Fretwell S D (1974). The optimal balance between size and number of offspring. The American Naturalist 108: 499506. Thompson K, Band S R, Hodgson J G (1993). Seed size and shape predict persistence in soil. Functional Ecology 7: 236-241. Urbieta I R, Pérez-Ramos I M, Zavala M A, Marañón T, Kobe R K (2008). Soil mater content and emergence time control seedling establishment on three co-occurring Mediterranean oak species. Canadian Journal of Forest Research 38: 23822393. Vaughton G, Ramsey M (1998). Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). Journal of Ecology 86: 563-573. Westoby M, Falster D S, Moles A T, Vesk P A, Wright I J (2002). Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33: 125-159. 25 Svensk sammanfattning Växter investerar stora resurser i reproduktion och frösättning, och storleken på frön har effekter på, exempelvis, groning och etablering. Från en given mängd resurser avsatta för fröproduktion, gör växter en avvägning mellan att producera ett stort antal små frön eller att producera ett litet antal stora frön. Stora frön innehåller en stor mängd lagrad energi, vilket gör att groddplantor som gror från stora frön är stora och kan klara av påfrestningar under etableringen väl. Exempelvis har man funnit att storfröiga arter har högre överlevnad än småfröiga arter om de utsätts för skuggning eller konkurrens från andra arter under etableringsfasen. Därmed har stora frön hög sannolikhet att etableras. Små frön, däremot, kan produceras i stort antal, och har därmed hög sannolikhet att kunna spridas till platser som är fria från konkurrens från andra växter. Eftersom stora frön har högre sannolikhet för etablering än små frön, särskilt under påfrestande förhållanden, kan man förvänta sig att stora frön skulle ha en fördel över små frön i slutna habitat, t ex skog, där det råder skuggiga förhållanden och ofta hård konkurrens mellan växter. Här skulle alltså sorteringsprocesser eller selektionsprocesser kunna göra att stora frön gynnas. Att producera stora frön innebär dock kostnader för växter, eftersom då endast ett relativt litet antal frön kan produceras. Dessutom löper stora frön ofta högre risk att bli uppätna av fröpredatorer, som smågnagare. I öppna habitat, t ex gräsmarker, råder oftast inte skuggiga förhållanden, och konkurrensen mellan växter är oftast låg, till följd av att störning, t ex betning, hindrar annars konkurrenskraftiga arter att ta över. Därmed skulle små frön kunna gynnas i öppna habitat, eftersom fördelen med att producera många lättspridda frön här väger tyngst. I växtvärlden varierar fröstorleken från ca. en miljondels gram till ca 10 kilo. Även inom växtsamhällen förekommer en betydande 26 fröstorleksvariation. Inom arter, och till och med inom individer, förekommer dessutom ofta en variation i fröstorlek. Hur denna stora variation i fröstorlek kan förekomma, och hur arter med olika stora frön kan samexistera kan anses förbryllande. Hur kan flera olika fröstorleksstrategier vara lika väl anpassade? Borde inte en viss fröstorlek vara den optimala? Olika modeller har försökt förklara samexistensen av arter med olika stora frön. Å ena sidan kan avvägningen mellan att producera ett litet antal stora frön eller ett stort antal små frön kopplas ihop med en avvägning mellan att vara en god konkurrent eller att vara en god kolonisatör. I denna modell kan stora frön etableras till följd av att de är goda konkurrenter och kan konkurrera ut alla mindre frön på en groningsplats. Små frön kan däremot etableras till följd av att de är goda kolonisatörer och kan finna groningsplatser som är obesatta av större frön. Å andra sidan kan avvägningen mellan att producera ett litet antal stora frön eller ett stort antal små frön även kopplas ihop med en avvägning mellan att vara stresstålig eller att ha hög fekunditet, dvs att frön produceras i stort antal. I denna modell gynnas stora frön i påfrestande miljöer, eftersom stora frön har mer lagrad energi och bättre kan klara av påfrestande förhållanden. Små frön, däremot, gynnas i miljöer med låg påfrestning till följd av att de förekommer i störst antal. I denna avhandling har jag försökt ta reda på hur rekryteringsmönster styrs av fröstorlek och habitat. Detta har jag gjort genom att studera om etablering påverkas av fröstorlek, både på mellanartsnivå och inomartsnivå, samt om det finns någon skillnad i hur denna påverkan ser ut i olika habitat. Jag har även studerat om det finns något samband mellan fröstorlek och fröpredation, och hur detta skiljer sig mellan habitat. Dessa studier har utförts i fält, i Tullgarns naturreservat och i Angarns naturreservat. För att studera hur etablering påverkas av fröstorlek mellan arter sådde jag ut frön av 20 arter i sex olika naturtyper som representerar en gradient från öppet habitat till slutet habitat. För att studera hur etablering påverkas av fröstorlek inom arter sådde jag ut frön från fyra olika arter i två olika naturtyper – gräsmark och lövskog. Dessa frön hade först vägts ett och ett, och såddes sedan också ett och ett, så att jag kunde hålla reda på varje enskilt frö. Groning och etablering för 27 samtliga utsådda frön följdes sedan upp till tre år. För att studera hur fröpredation påverkas av fröstorlek lade jag ut frön från tio olika arter i två olika habitat – gräsmark och lövskog. Frön placerades ut ett och ett, och efter 48 timmar läste jag av vilka frön som försvunnit. Detta upprepades sju gånger på sammanlagt tio lokaler. Jag har även studerat om stora frön har en fördel över små frön vid samexistens med varandra. Denna studie utfördes i en bänkgård på Stockholms universitets campus, dvs under kontrollerade förhållanden, med frön sådda i krukor. I studien ingick 14 arter som delades in i sju par, där varje par bestod av en storfröig och en småfröig art. Frön från båda arterna inom ett par såddes tillsammans i krukor med 25 frön av varje art eller 50 frön av varje art, och utsattes för sex olika behandlingar med förna och skuggning. Groning och etablering förljdes under två år. Resultaten från de båda utsåningsförsöken i fält visade att groning och rekrytering påverkas positivt av fröstorlek, men att effekten av fröstorlek är ganska svag. I vissa fall kunde en effekt av habitat även ses, så att den positiva effekten av stora frön blev starkare i slutna habitat (skog) än i öppna habitat (gräsmark), men denna effekt uteblev i andra fall. Detta kan bero på att variationer i abiotiska fröhållanden (t ex torka) mellan olika år kan ha en större effekt på groning och rekrytering än de skillnader som förekommer mellan olika habitat. Utifrån dessa resultat föreslår jag följande förklaringsmodell: 1) Under gynnsamma förhållanden (t ex i gräsmark under gynnsamma år) gror och etableras all frön lika bra oberoende av fröstorlek, och därmed syns ingen effekt av fröstorlek på groning och etablering. 2) Under mycket påfrestande förhållanden (t ex i sluten skog under torra år) gror och etableras alla frön lika dåligt, och därmed syns återigen ingen effekt av fröstorlek på groning och etablering. 3) Under intermediärt påfrestande förhållanden (t ex i gräsmark under torra år eller i skog under gynnsamma år) gynnas stora frön framför små frön, till följd av stora fröns bättre förmåga att klara av påfrestningar under etableringsfasen. Därmed uppkommer en positiv effekt av fröstorlek på groning och rekrytering. 28 Resultaten från fröpredationsexperimentet i fält visade att långt fler frön försvinner i slutna habitat (lövskog) än i öppna habitat (gräsmark). Detta var förväntat, eftersom slutna habitat antagligen erbjuder fler skyddade platser för fröpredatorer än öppna habitat. Resultaten visade även ett negativt samband mellan fröstorlek och andelen försvunna frön, dvs ju mindre frön desto större sannolikhet att försvinna. Detta resultat var oväntat, eftersom stora frön förväntas löpa större risk att bli uppätna. Detta oväntade resultat kan bero på att små frön lättare försvinner till följd av sekundär spridning (t ex blåser bort eller sprids av djur), snarare än faktisk förpredation. En annan förklaring kan vara att olika grupper av fröpredatorer föredrar olika fröstorlekar, så att exempelvis myror och sniglar föredrar små frön, medan smågnagare föredrar stora frön, förutsatt att de olika grupperna av fröpredatorer har olika förekomst. Om små frön har större risk att försvinna kan detta ha effekter på de rekryteringsmönster funna i de båda utsåningsförsöken i fält. Det positiva sambandet mellan fröstorlek och rekrytering, dvs att stora frön har större sannolikhet att etableras, skulle alltså kunna vara en effekt av att små frön i högre grad försvinner. Resultaten från bänkgårdsexperimentet visade att stora frön generellt har en fördel över små frön i direkt tävling om groningsplatser. Denna fördel ökade i behandlingar med förna. Skuggning hade endast svag effekt på fördelen av stora frön, och då snarast så att stora frön gynnades mer i behandlingar utan skugga jämfört med behandlingar med skugga. Däremot fann jag ingen effekt av frötäthet på fördelen av stora frön, dvs fördelen som stora frön hade över små frön var densamma oavsett om frön hade såtts glest (25 frön av varje art) eller tätt (50 frön av varje art). Dessa resultat ger stöd för modeller för samexistens av arter med olika fröstorlek, så tillvida att stora frön har en fördel över små frön. I en modell baserad på en avvägning mellan konkurrens och kolonisation skulle man förvänta sig att stora frön skulle gynnas mer i hög frötäthet än i låg frötäthet, till följd av att många frön då skulle konkurrera om ett begränsat antal groningsplatser – en tävling som de stora fröna skulle vinna. Jag fann dock lite stöd för en sådan modell, eftersom frötäthet inte 29 hade någon effekt på storfröiga arters fördel. Däremot fann jag visst stöd för en modell baserad på en avvägning mellan stresstolerans och fekunditet, eftersom stora frön gynnades mer i behanlingar med förna än i behandlingar utan förna. Att ta sig igenom ett förnalager innebär en påfrestning för groddplantor som gror i habitat med tjockt förnalager, och en sådan påfrestning skulle alltså kunna vara avgörande för vilka arter som lyckas etableras. Jag fann även en svag effekt av att stora frön gynnades mer i behandlingar utan skugga än i behandlingar med skugga. Detta skulle kunna bero på att skuggväven som användes i fösöken för att skapa skugga, även hade en isolerande effekt så att frön som skuggades fick ett lite mer gynnsamt mikroklimat och inte blev uttorkade lika lätt som oskuggade frön. Även detta ger visst stöd för en modell baserad på en avvägning mellan tolerans och fekunditet, där stora frön förväntas ha fördel över små frön i påfrestande förhållanden. Sammanfattningsvis finns alltså ett rekryteringsmönster där rekrytering påverkas positivt av fröstorlek, och där denna effekt är starkare i slutna habitat än i öppna habitat. Effekterna av fröstorlek och, särskilt, habitat är dock svaga, och faktorer som exempelvis variationer i väderlek mellan år kan ha större effekter på rekrytering. Ett rekryteringsmönster med ett positivt samband mellan fröstorlek och etablering kan vara en effekt av att små frön i högre grad försvinner till följd av fröpredation eller sekundär spridning. Under kontrollerade förhållanden finns dock en tydlig fördel av stora frön över små frön – en fördel som ökar vid påfrestande förhållanden. 30 Tack! Under sju och ett halvt år har botan varit min arbetsplats, och min doktorandtid här har varit fantastisk, mycket tack vare alla sköna människor. Jag trivs otroligt bra på botan, och det har känts roligt att åka till jobbet varje dag. Först och främst vill jag tacka min handledare Ove Eriksson. Tack för att du alltid haft tid, för att du alltid läst och kommenterat manus så snabbt och för din otroliga förmåga att se de enkla sambanden. Tack för att jag med din handledning fått möjlighet att växa! Jag vill också tacka min biträdande handledare Kjell Bolmgen. Tack för inspirerande diskussioner om allt från de stora ekologiska frågorna till film och litteratur. Tack alla room-mates i rum 539 som förgyllt tillvaron. Tack Didrik och Hugo för alla roliga diskussioner om allt som rör ekologi, och lite till. Tack Mathias, du var också med. Tack myrorna. Tack Malin, för kul hästsnack. Tack Ellen. För allt! Tack Rammstein. Rum 540 – förlåt. Tack Lenn, din gulkämpar-föreläsning fick mig att inse att det var växtekolog jag ville bli. Tack Jocke, för delad förvirring i början. Tack Tove och Helena, för delad ångest på slutet. Tack Petter, för ditt lugn och för det bästa (och självklaraste) rådet under hela doktorandtiden: ”det är bara att skriva tills det är klart”. Tack Lisa och Lina för sköna pubar. Tack Tove, för mysigt ressällskap. Tack Gundula, för din cynism. Tack Peter och Ingela för råd och hjälp i växthuset och bänkgården, samt för trevliga pratstunder. Tack alla vuxna, post-docs, doktorander, assistenter och ex-jobbare genom åren, för att ni gör växtekologiska avdelningen till en sådan stimulerande miljö. Jag kommer sakna er alla! Tack alla assistenter som hjälpt till med de olika projekten. Utan er hade detta inte varit möjligt. Tack Irja för insamling och hjälp med utsåning av 300.000 frön. Tack Lena, för avläsning och utsåning, men också för svamp, mögelost och trevligt sällskap på Tullbotorp. Tack Maria, för 31 utsåning och vägning av frön, trots att du var lika gravid som jag. Tack Samira och Malin S, för avläsningar i fält och i bänkgården. Tove, du var också med på ett hörn. Tack mamma och pappa för stöd och uppmuntran. Tack Jessica. Tack stalltjejerna och hästarna på Örsta. Tack Patrik. Du höll mig under armarna när det var jobbigt. Utan dig hade det inte blivit någon avhandling. pok. Tack Ida och Gustav. Ni är det finaste och viktigaste av allt ♥ Nu kommer mamma ut ur bubblan. 32