Angela T. Moles

The evolutionary ecology of seed size.

Seed mass is a trait that occupies a pivotal position in the ecology of a species. It links the ecology of reproduction and seedling establishment with the ecology of vegetative growth, strategy sectors that are otherwise largely disconnected (Grime et al., 1988; Shipley et al., 1989; Leishman and Westoby, 1992). There is a startling diversity of shapes and sizes of seeds among the plant species of the world. Seeds range from the dust seeds of the Orchidaceae and some saprophytic and parasitic species (around 10 6 g), across ten orders of magnitude to the double coconut Lodoicea seychellarum (104 g) (Harper et al., 1970). Within species, seed size typically spans less than half an order of magnitude (about fourfold: Michaels et al., 1988). Most within-species variation occurs within plant rather than among plants or populations (Michaels et al., 1988; Obeso, 1993; Vaughton and Ramsey, 1998), indicating environmental effects during development rather than genetic differences between mothers. This chapter is concerned with the differences in seed size among species, and the consequences for vegetation dynamics and community composition. During the last 10–15 years, there has been considerable progress in the ecology of seed mass. Unlike many other areas of comparative plant ecology, we have substantial published information from several different scales and research styles. As well as field experiments and demographic studies with a few species at a time, we have simple experiments with larger numbers of species (ten to 50), quantification of seed mass and its correlates in whole-vegetation types (hundreds of species) and tests of consistency across different continents. The wide-scale quantification began as early as Salisbury (1942) and Baker (1972), but has been much added to and consolidated over the past 10 years (e.g. Mazer, 1989, 1990; Leishman and Westoby, 1994a; Leishman et al., 1995; Eriksson and Jakobsson, 1998). The work spanning large numbers of species is complementary to detailed experiments involving only a few species, giving a stronger sense of how widely the results from particular experiments can be generalized. Much of the literature examines how natural selection on seed size might be influenced by various environmental factors. In this context, it is at first glance surprising that seed size varies within communities across a remarkable five to six orders of magnitude (Leishman et al., 1995; Fig. 2.1). Further, there is strong overlap of seed-size distributions between quite different habitats. Within the temperate zone,

Three keys to the radiation of angiosperms into freezing environments

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species’ traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

The global spectrum of plant form and function

Earth is home to a remarkable diversity of plant forms and life histories, yet comparatively few essential trait combinations have proved evolutionarily viable in today’s terrestrial biosphere. By analysing worldwide variation in six major traits critical to growth, survival and reproduction within the largest sample of vascular plant species ever compiled, we found that occupancy of six-dimensional trait space is strongly concentrated, indicating coordination and trade-offs. Three-quarters of trait variation is captured in a two-dimensional global spectrum of plant form and function. One major dimension within this plane reflects the size of whole plants and their parts; the other represents the leaf economics spectrum, which balances leaf construction costs against growth potential. The global plant trait spectrum provides a backdrop for elucidating constraints on evolution, for functionally qualifying species and ecosystems, and for improving models that predict future vegetation based on continuous variation in plant form and function.

DO SMALL‐SEEDED SPECIES HAVE HIGHER SURVIVAL THROUGH SEED PREDATION THAN LARGE‐SEEDED SPECIES?

Seed ecologists have often stated that they expect larger-seeded species to have lower survivorship through postdispersal seed predation than smaller-seeded species. Similar predictions can be made for the relationship between survivorship through predis- persal seed predation and seed mass. In order to test these predictions, we gathered data regarding survivorship through 24 hours of exposure to postdispersal seed predators for 81 Australian species, and survivorship through predispersal seed predation for 170 Aus- tralian species. These species came from an arid environment, a subalpine environment, and a temperate coastal environment. We also gathered data from the published literature (global) on survivorship through postdispersal seed predation for 280 species and survi- vorship through predispersal seed predation for 174 species. We found a weak positive correlation between seed mass and the percentage of seeds remaining after 24 hours of exposure to postdispersal seed predators at two of three field sites in Australia, and no significant relationship across 280 species from the global lit- erature, or at the remaining field site. There was no significant relationship between seed mass and survivorship through predispersal seed predation either cross-species or across phylogenetic divergences in any of the vegetation types, or in the compilation of data from the literature. Postdispersal seed removal was responsible for a greater percentage of seed loss in our field studies than was predispersal seed predation. On average, 83% of diaspores remained after 24 hours of exposure to postdispersal seed removers, whereas 87% of seeds survived all predispersal seed predation that occurred between seed formation and seed maturity. Mean seed survival was higher in the field studies than in the literature compi- lations, and species showing 100% survival were heavily underrepresented in the literature. These differences may be due to biases in species selection or publication bias. Seed defensive tissue mass increased isometrically with seed mass, but there was no significant relationship between the amount of defensive tissue per gram of seed reserve mass and survivorship through postdispersal seed predation.

Alternative stable states in Australia’s Wet Tropics: a theoretical framework for the field data and a field-case for the theory

The vegetation of the Wet Tropics bioregion of Far North Queensland is a complex system whose components (mainly tropical rainforests and fire-prone forests and woodlands) have mostly been studied independently from each other. We suggest that many characteristics of the vegetation are consistent with those of a complex, dynamic, spatially heterogeneous system which exhibits alternative stable states. We propose these states are driven and maintained by the interaction of vegetation-specific positive feedback loops with the regions’ environmental parameters (such as topography, steep humidity gradients and seasonality) and result in the rainforest/fire-prone vegetation mosaic that characterises the area. Given the regions’ magnitude, biodiversity and complexity, we propose the Wet Tropics as an important new example and a good testing ground for alternative stable state and resilience theories in large heterogeneous natural systems. At the same time, thinking in terms of alternative stable states and resilience creates a new context for understanding the regions’ biological dynamics.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Fossil leaf economics quantified: calibration, Eocene case study, and implications

Abstract Leaf mass per area (MA) is a central ecological trait that is intercorrelated with leaf life span, photosynthetic rate, nutrient concentration, and palatability to herbivores. These coordinated variables form a globally convergent leaf economics spectrum, which represents a general continuum running from rapid resource acquisition to maximized resource retention. Leaf economics are little studied in ancient ecosystems because they cannot be directly measured from leaf fossils. Here we use a large extant data set (65 sites; 667 species-site pairs) to develop a new, easily measured scaling relationship between petiole width and leaf mass, normalized for leaf area; this enables MA estimation for fossil leaves from petiole width and leaf area, two variables that are commonly measurable in leaf compression floras. The calibration data are restricted to woody angiosperms exclusive of monocots, but a preliminary data set (25 species) suggests that broad-leaved gymnosperms exhibit a similar scaling. Application to two well-studied, classic Eocene floras demonstrates that MA can be quantified in fossil assemblages. First, our results are consistent with predictions from paleobotanical and paleoclimatic studies of these floras. We found exclusively low-MA species from Republic (Washington, U.S.A., 49 Ma), a humid, warm-temperate flora with a strong deciduous component among the angiosperms, and a wide MA range in a seasonally dry, warm-temperate flora from the Green River Formation at Bonanza (Utah, U.S.A, 47 Ma), presumed to comprise a mix of short and long leaf life spans. Second, reconstructed MA in the fossil species is negatively correlated with levels of insect herbivory, whether measured as the proportion of leaves with insect damage, the proportion of leaf area removed by herbivores, or the diversity of insect-damage morphotypes. These correlations are consistent with herbivory observations in extant floras and they reflect fundamental trade-offs in plant-herbivore associations. Our results indicate that several key aspects of plant and plant-animal ecology can now be quantified in the fossil record and demonstrate that herbivory has helped shape the evolution of leaf structure for millions of years.

Potential contributions of the seed rain and seed bank to regeneration of native forest under plantation pine in New Zealand

The seed rain, seed bank, and vegetatio n were studied in a Pinus radiata plantation destined for restoration to native forest, in order to gain in - formation on the vegetation dynamics and potential future vegetation composition of this forest. A total of 1812 ± 245 seeds m-2from 34 species fell in the seed rain between October 1996 and May 1997 . The seed bank had a density of 8841 ± 1157 seeds m 2 , and contained at least 45 species. Alien species con- tributed 2% of the seedlings and saplings, 6% of th e adults, 9% of the seed rain, and 30% of the see d bank, and accounted for 28 of the 69 species identi- fied in this study. As long as disturbance to the for- est is minimal, native species can be expected t o dominate regeneration. However, only 30 species o f seed plants were present as seedlings, saplings, o r adults, and several late-successional native specie s have become locally extinct . The seed rain is a po- tential source of recruits for these species (12 of the 34 species found in the seed rain were not presen t in the vegetation), but some species will need to be actively reintroduced if the forest is to be returne d to its pre-human condition .

Functional distinctiveness of major plant lineages

Summary Plant traits vary widely across species and underpin differences in ecological strategy. Despite centuries of interest, the contributions of different evolutionary lineages to modern-day functional diversity remain poorly quantified. Expanding data bases of plant traits plus rapidly improving phylogenies enable for the first time a data-driven global picture of plant functional diversity across the major clades of higher plants. We mapped five key traits relevant to metabolism, resource competition and reproductive strategy onto a phylogeny across 48324 vascular plant species world-wide, along with climate and biogeographic data. Using a novel metric, we test whether major plant lineages are functionally distinctive. We then highlight the trait–lineage combinations that are most functionally distinctive within the present-day spread of ecological strategies. For some trait–clade combinations, knowing the clade of a species conveys little information to neo- and palaeo-ecologists. In other trait–clade combinations, the clade identity can be highly revealing, especially informative clade–trait combinations include Proteaceae, which is highly distinctive, representing the global slow extreme of the leaf economic spectrum. Magnoliidae and Rosidae contribute large leaf sizes and seed masses and have distinctively warm, wet climatic distributions. Synthesis. This analysis provides a shortlist of the most distinctive trait–lineage combinations along with their geographic and climatic context: a global view of extant functional diversity across the tips of the vascular plant phylogeny.

Seedling Ecology and Evolution: The seedling as part of a plant's life history strategy

In this chapter, we will describe the intricate links between seedling ecology and life history traits such as seed mass, time to maturity, adult size, and reproductive life span. We will pay particular attention to seed mass, as this is the trait most closely linked to seedling ecology. Seed mass affects the initial size of the seedlings, the amount of reserves seedlings have for establishment, the sites to which seeds are dispersed, and the time seeds spend in the soil before germinating. Much of our understanding of seed and seedling ecology has been based on the idea that plants face a trade-off between producing a few large seeds, each with high rates of survival as seedlings, versus producing many small seeds, each with lower rates of survival as seedlings. We, therefore, begin by reviewing the evidence for this trade-off. Our review shows that a full understanding of seed and seedling ecology requires consideration of life history variables such as plant height, reproductive life span, and the length of the juvenile period. Then we present a new framework for understanding seed and seedling traits as part of an overall life history strategy. Next we outline relationships between seed and seedling traits and other aspects of plant ecological strategy, such as seed dispersal syndrome, the capability to form soil seed banks, tissue density, and adult plant traits. These data complement previous results, and tend to support the idea that seed and seedling traits can be usefully understood as part of a larger spectrum of life history traits ranging from small, short-lived plants with small seeds, fast growth, low tissue density, and low rates of seedling survival to large, long-lived plants with large seeds, slower growth, denser tissues, and higher rates of survival. Our focus in this chapter is mostly on between-species variation in seed and seedling strategies. This is because the vast majority of the variation in these traits lies at the between-species level. Across all of the species on earth, seed mass ranges over 11.5 orders of magnitude