Susan J. Mazer

POLLEN LIMITATION OF PLANT REPRODUCTION: ECOLOGICAL AND EVOLUTIONARY CAUSES AND CONSEQUENCES

Determining whether seed production is pollen limited has been an area of intensive empirical study over the last two decades. Yet current evidence does not allow satisfactory assessment of the causes or consequences of pollen limitation. Here, we critically evaluate existing theory and issues concerning pollen limitation. Our main conclusion is that a change in approach is needed to determine whether pollen limitation reflects random fluctuations around a pollen–resource equilibrium, an adaptation to stochastic pollination environments, or a chronic syndrome caused by an environmental perturbation. We formalize and extend D. Haig and M. Westobys conceptual model, and illustrate its use in guiding research on the evolutionary consequences of pollen limitation, i.e., whether plants evolve or have evolved to ameliorate pollen limitation. This synthesis also reveals that we are only beginning to understand when and how pollen limitation at the plant level translates into effects on plant population dynamics...

Warming experiments underpredict plant phenological responses to climate change

Warming experiments are increasingly relied on to estimate plant responses to global climate change. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.

Are functional traits good predictors of demographic rates? Evidence from five neotropical forests

A central goal of comparative plant ecology is to understand how functional traits vary among species and to what extent this variation has adaptive value. Here we evaluate relationships between four functional traits (seed volume, specific leaf area, wood density, and adult stature) and two demographic attributes (diameter growth and tree mortality) for large trees of 240 tree species from five Neotropical forests. We evaluate how these key functional traits are related to survival and growth and whether similar relationships between traits and demography hold across different tropical forests. There was a tendency for a trade-off between growth and survival across rain forest tree species. Wood density, seed volume, and adult stature were significant predictors of growth and/or mortality. Both growth and mortality rates declined with an increase in wood density. This is consistent with greater construction costs and greater resistance to stem damage for denser wood. Growth and mortality rates also declined as seed volume increased. This is consistent with an adaptive syndrome in which species tolerant of low resource availability (in this case shade-tolerant species) have large seeds to establish successfully and low inherent growth and mortality rates. Growth increased and mortality decreased with an increase in adult stature, because taller species have a greater access to light and longer life spans. Specific leaf area was, surprisingly, only modestly informative for the performance of large trees and had ambiguous relationships with growth and survival. Single traits accounted for 9-55% of the interspecific variation in growth and mortality rates at individual sites. Significant correlations with demographic rates tended to be similar across forests and for phylogenetically independent contrasts as well as for cross-species analyses that treated each species as an independent observation. In combination, the morphological traits explained 41% of the variation in growth rate and 54% of the variation in mortality rate, with wood density being the best predictor of growth and mortality. Relationships between functional traits and demographic rates were statistically similar across a wide range of Neotropical forests. The consistency of these results strongly suggests that tropical rain forest species face similar trade-offs in different sites and converge on similar sets of solutions.

Ecological, Taxonomic, and Life History Correlates of Seed Mass Among Indiana Dune Angiosperms

This study evaluated the ecological and taxonomic correlates of seed mass variation among 648 angiosperm species of the Indiana Dunes region (1 13 families, 507 genera in the original flora). The sample represented 50% of the species, 60% of the genera, and 67% of the families reported from the area. Species were chosen at random from the published flora. Each species was characterized by family membership, habitat, life history, phenological characters, and native vs. alien status, in order to determine the relationship among species between these variables and mean seed mass. Unique to this study are measurements of the effects of phenology and taxonomic family on seed mass. Each species occurred in - 1 of 13 habitat types described in the Indiana Dunes flora. To determine the effect of apparent water and light availability on seed mass, each habitat was assigned to one of four categories representing combinations of inferred water and light availability. Life histories or life forms represented were: annuals, biennials, herbaceous vines, parasites, perennials, short-lived perennials, shrubs, small trees, trees, and woody vines. Two phenological variables were available for most species: the time at which flowering begins (early, middle, or late), and the duration of flowering (short: 3 mo). The mean seed mass of each species was established by weighing samples from herbarium specimens in the United States National Herbarium. The frequency distribution of raw seed mass is highly skewed among species, so mean seed mass for each species was assigned to 1 of 14 seed mass classes based on a log scale (cf. Baker 1972). This transformation achieved a nearly normal distribution and made the data presentation comparable to that of Baker. One-way ANOVAs measured the effects of each factor across all other variables; two-way ANOVAs were conducted to detect significant interactions and strong associations between characters; multi-factorial ANOVAs were performed to measure the effect of each class variable independent of the others and to corroborate associations between characters suggested by the two-way ANOVAs. One-way ANOVAs revealed a statistically significant effect of all ecological and taxonomic factors on seed mass, with the exception of native vs. alien status. Seed mass variance was accounted for as follows: family, 30%; life history, 22%; habitat, 8%; water/light category, 5%; onset of flowering, 5%; and duration of flowering, 4%. The smallest seeds were produced by the Scrophulariaceae and the largest by the Fabaceae, Liliaceae, and Rosaceae. The largest seeded species lived in closed habitats: wooded dunes, thickets, and wet dunes. Small- seeded species were associated with open habitats: wet dunes, aquatic habitats, marshes, and streamsides. Light availability was a better predictor of relative seed mass than was inferred water availability. The strong effect of life history on seed mass was due primarily to the extremely large seeds produced by trees. Significant differences in seed mass were not detected among life forms producing seeds of intermediate mass (seeds produced by annuals, biennials, perennials, shrubs, small trees, and vines were statistically indistinguishable). Early flowering and flowering of short duration were associated with the production of large seeds. Two-way ANOVAs detected eight significant two-way interactions: family x native vs. alien status, family x life history, family x onset of flowering, habitat x life history, water/light category x life history, water/ light category x native vs. alien status, life history x duration of flowering, and onset of flowering x duration of flowering. These were further evaluated to determine the source of the interaction. Multi-factorial ANOVAs provided measurements of the effects of one class variable on seed mass while all other variables were controlled statistically. The statistical effect on seed mass of each variable independent of the others was much lower than in the one-way ANOVAs. Seed mass variance was explained independently by each variable as follows: family, 13%; life history, 13%; habitat, 4%; water/light category, 3%; onset of flowering, 1 %; and duration of flowering, 1%. Two strong associations were detected in these ANOVAs: an association between family and habitat, and between life history and onset of flowering. Although the effects of ecological and life history characters on seed mass evaluated in this study were highly statistically significant, the R2 values associated with these effects were quite low. For example, habitat accounted for only 4% of the variance in seed mass independent of the other effects measured. This suggests that at the geographic scale investigated in this study, there is no primary habitat-specific ecological attribute that determines the seed mass of a habitats component species. Seed mass of a species is determined by a combination of its

Parental effects on seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection

The possibility that sexual selection operates in angiosperms to effect evolutionary change in polygenic traits affecting male reproductive success requires that there is additive genetic variance for these traits. I applied a half‐sib breeding design to individuals of the annual, hermaphroditic angiosperm, wild radish (Raphanus raphanistrum: Brassicaceae), to estimate paternal genetic effects on, or, when possible, the narrow‐sense heritability of several quantitative traits influencing male reproductive success. In spite of significant differences among pollen donors with respect to in vitro pollen tube growth rates, I detected no significant additive genetic variance in male performance with respect to the proportion of ovules fertilized, early ovule growth, the number of seeds per fruit, or mean individual seed weight per fruit. In all cases, differences among maternal plants in these traits far exceeded differences among pollen donors. Abortion rates of pollinated flowers and fertilized ovules also differed more among individuals as maternal plants than as pollen donors, suggesting strong maternal control over these processes. Significant maternal phenotypic effects in the absence of paternal genetic or phenotypic effects on reproductive traits may be due to maternal environmental effects, to non‐nuclear or non‐additive maternal genetic effects, or to additive genetic variance in maternal control over offspring development, independent of offspring genotype. While I could not distinguish among these alternatives, it is clear that, in wild radish, the opportunity for natural or sexual selection to effect change in seed weight or seed number per fruit appears to be greater through differences in female performance than through differences in male performance.

CONSTANCY OF POPULATION PARAMETERS FOR LIFE‐HISTORY AND FLORAL TRAITS IN RAPHANUS SATIVUS L. II. EFFECTS OF PLANTING DENSITY ON PHENOTYPE AND HERITABILITY ESTIMATES

To determine the effect of growing conditions on population parameters in wild radish, (Raphanus sativus L.: Brassicaceae), we replicated maternal and paternal half‐sib families of seed across three planting densities in an experimental garden. A nested breeding design performed in the greenhouse produced 1,800 F1 seeds sown in the garden. We recorded survivorship, measured phenotypic correlations among and estimated narrow‐sense and broad‐sense heritabilities (h2) of: days to germination, days to flowering, petal area, ovule number/flower, pollen production/flower, and modal pollen grain volume. Survivorship declined with increasing density, but the relative abundances of surviving families did not differ significantly among densities. Seeds in high‐density plots germinated significantly faster than seeds sown in medium‐ or low‐density plots, but they flowered significantly later. Plants in high‐density plots had fewer ovules per flower than those in the other treatments. Petal area and pollen characters did not differ significantly among densities. Densities differed with respect to the number and sign of significant phenotypic correlations. Analyses of variance were conducted to detect additive genetic variance (Va) of each trait in each density. At low density, there were significant paternal effects on flowering time and modal pollen grain volume; in medium‐density plots, germination time, flowering time and ovule number exhibited significant paternal effects; in high‐density plots, only pollen grain volume differed among paternal sibships. The ability to detect maternal effects on progeny phenotype also depended on density. Narrow‐sense h2 estimates differed markedly among density treatments for germination time, flowering time, ovule number and pollen grain volume. Maternal, paternal and error variance components were estimated for each trait and density to examine the sources of variation in narrow‐sense h2 across densities. Variance components did not change consistently across densities; each trait behaved differently. To provide qualitative estimates of genetic correlations between characters, correlation coefficients were estimated using paternal family means; these correlations also differed among densities. These results demonstrate that: a) planting density influences the magnitude of maternal and paternal effects on progeny phenotype, and of h2 estimates, b) traits differ with respect to the density in which heritability is greatest, c) density affects the variance components that comprise heritability, but each trait behaves differently, and d) the response to selection on any target trait should result in different correlated responses of other traits, depending on density.

Gametophytic selection in Raphanus raphanistrum: a test for heritable variation in pollen competitive ability

Competition among many microgametophytes for a limited number of ovules can lead to both nonrandom fertilization by pollen genotypes and selection for greater sporophytic vigor. The evolutionary implications of this process depend on the extent of heritable genetic variation for pollen competitive ability. Using flower color in wild radish as a genetic marker, we demonstrate differences among pollen donors in competitive ability. Significant differences were found in four out of five pairs of donors. For three pairs of donors, competitive differences were observed in certain maternal plants but not others.

Angiosperm growth habit, dispersal and diversification reconsidered

SummaryPrevious studies have sought to elucidate the relationship between dispersal mode (biotic versus abiotic) and the taxonomic diversification of angiosperm families, but with ambiguous results. In this study, we propose the hypothesis that the combination of (1) the large seed size required of plants germinating in closed, light-poor environments and (2) the necessity to move disseminules away from the maternal plant in order to avoid intraspecific competition, predation and pathogens should favour biotically-dispersed relative to abiotically-dispersed woody arborescent angiosperms, resulting in higher diversification of the former. In this paper, we seek patterns of diversification that support this hypothesis. We examine the association between dispersal mode, growth habit and taxonomic richness of monocotyledon and dicotyledon families using (1) contingency table analyses to detect the effect of dispersal mode on the relative abundances and diversification of woody versus herbaceous taxa and (2) non-parametric analyses of variance to detect the statistical effect of dispersal mode on taxonomic diversification (mean number of species per genus, genera per family and species per family) in monocot and dicot families dominated by biotic or abiotic dispersal. We found a clear statistical effect of dispersal mode on diversification. Among families of woody dicots, dispersal by vertebrates is associated with significantly higher levels of species per genus, genera per family and species per family than is abiotic dispersal. The same pattern is observed among woody monocots, but is not significant at the 0.05 level. Among families of herbaceous monocots and dicots, the situation is reversed, with abiotically-dispersed families exhibiting higher levels of diversification than vertebrate-dispersed families. When woody and herbaceous families are pooled, there is no association between dispersal mode and diversification. These data coincide with evidence from the fossil record to suggest vertebrate dispersal has positively contributed to the diversification of woody angiosperms. We suggest that vertebrate dispersal may have promoted the diversity of extant taxa by reducing the probability of extinction over evolutionary time, rather than by elevating speciation rates. Our results suggest vertebrate dispersal has contributed to, but does not explainin toto, the diversity of living angiosperms.

Seed mass of Indiana Dune genera and families: Taxonomic and ecological correlates

SummarySeveral surveys have documented an association among species between habitat type and seed mass, suggesting that habitat attributes impose a direct selective force on seed mass. Previous comparative surveys, however, have not controlled for the statistical effects of shared phylogenetic history (at the genus or family level) and life form when evaluating the relationship between habitat and seed mass. This study of the Indiana Dunes angiosperm flora provides statistical ‘control’ of genus and family membership by: (i) partitioning out the statistical effect of genus membership prior to measuring the effect of habitat on seed mass, and (ii) seeking an association between habitat and seed mass within eight genera (206 species) and ten families (366 species). To measure the associations between ecological factors, taxonomic membership and seed mass, I examined life form, phenological schedules and seed mass among species in 8 genera distributed among 13 habitat types (assigned to 1 of 4 categories of inferred water and light availability). One-way ANOVAS indicated that genus, life form, habitat, water/light category, the onset of flowering and the duration of flowering accounted for 71%, 51%, 10%, 4%, 14% and 14% of the variance in seed mass, respectively. However, multi-factor ANOVAS measured the variance in seed mass accounted for by each variable independently of the others: only genus explained a significant proportion (11%). Genus membership is strongly associated with the other ecological factors, accounting for the difference between one-way and multi-factor ANOVAS. Within the ecologically widespread genera and families of this study, there was no significant association between water/light category and seed mass, even though this association can be detected across taxa. Among congeners and confamilials, interspecific variation in seed mass (measured as the coefficient of variation) was as high within habitat types as among them, suggesting that habitats do not provide upper limits to the range of seed mass exhibited by the species within them. A previous study of 648 Indiana Dune species showed that species segregate among habitats on the basis of seed size; large-seeded species tend to occupy closed habitats and small-seeded species tend to inhabit open habitats. This segregation creates the ecologically meaningful observation that low-light habitats support larger-seeded species than high-light habitats, even though this pattern cannot be detected independently of taxonomic membership. Generalist taxa may occupy a wide range of habitats for reasons other than their seed size. If this is a common feature of ecological generalists, it may not be possible to detect an association between habitat and seed size independently of taxonomic membership.

Phylogenetic conservatism in plant phenology

Summary 1. Phenological events – defined points in the life cycle of a plant or animal – have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. 2. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. 3. Here, we evaluated evidence for phylogenetic conservatism – the tendency for closely related species to share similar ecological and biological attributes – in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing ~4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the set of included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. 4. We show that more closely related species tend to flower and leaf at similar times. By contrasting mean flowering times within and across sites, however, we illustrate that it is not the time of year that is conserved, but rather the phenological responses to a common set of abiotic cues. 5. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses. 6. Synthesis. Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conserved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species’ shared evolutionary histories.