Identifying predictors of translocation success in rare plant species.

The fundamental goal of a rare plant translocation is to create self-sustaining populations with the evolutionary resilience to persist in the long term. Yet, most plant translocation syntheses focus on a few factors influencing short-term benchmarks of success (e.g., survival and reproduction). Short-term benchmarks can be misleading when trying to infer future growth and viability because the factors that promote establishment may differ from those required for long-term persistence. We assembled a large (n = 275) and broadly representative data set of well-documented and monitored (7.9 years on average) at-risk plant translocations to identify the most important site attributes, management techniques, and species' traits for six life-cycle benchmarks and population metrics of translocation success. We used the random forest algorithm to quantify the relative importance of 29 predictor variables for each metric of success. Drivers of translocation outcomes varied across time frames and success metrics. Management techniques had the greatest relative influence on the attainment of life-cycle benchmarks and short-term population trends, whereas site attributes and species' traits were more important for population persistence and long-term trends. Specifically, large founder sizes increased the potential for reproduction and recruitment into the next generation, whereas declining habitat quality and the outplanting of species with low seed production led to increased extinction risks and a reduction in potential reproductive output in the long-term, respectively. We also detected novel interactions between some of the most important drivers, such as an increased probability of next-generation recruitment in species with greater seed production rates, but only when coupled with large founder sizes. Because most significant barriers to plant translocation success can be overcome by improving techniques or resolving site-level issues through early intervention and management, we suggest that by combining long-term monitoring with adaptive management, translocation programs can enhance the prospects of achieving long-term success.

Identificación de pronosticadores del éxito de reubicación en especies raras de plantas Resumen El objetivo fundamental de la reubicación de plantas raras es la creación de poblaciones autosuficientes con resiliencia evolutiva que persistan a la larga. De todas maneras, la mayoría de las síntesis de estas reubicaciones se enfocan en unos cuantos factores que influyen sobre los parámetros a corto plazo del éxito (supervivencia y reproducción). Los parámetros a corto plazo pueden ser engañosos si se intenta inferir el crecimiento y la viabilidad en el futuro ya que los factores que promueven el establecimiento pueden diferir de aquellos requeridos para la persistencia a largo plazo. Ensamblamos un conjunto grande de datos representativos en general (n = 275) de las reubicaciones de plantas en riesgo bien documentadas y monitoreadas (7.9 años en promedio) para identificar los atributos de sitio más importantes, las técnicas de manejo y los rasgos de las especies para seis parámetros de ciclos de vida y medidas poblacionales del éxito de reubicación. Usamos el algoritmo de bosque aleatorio para cuantificar la importancia relativa de las 29 variables de pronosticadores para cada medida del éxito. Los factores en los resultados de las reubicaciones variaron con los marcos temporales y las medidas de éxito. Las técnicas de manejo tuvieron la mayor influencia relativa sobre la obtención de parámetros de ciclos de vida y tendencias poblacionales a corto plazo, mientras que los atributos de sitio y los rasgos de la especie fueron más importantes para la persistencia poblacional y las tendencias a largo plazo. En específico, las grandes cantidades de fundadores incrementaron el potencial de reproducción y reclutamiento de la siguiente generación, mientras que la declinación de la calidad del hábitat incrementó el riesgo de extinción y el trasplante de especies con baja producción de semillas redujo el rendimiento del potencial reproductivo a la larga. También detectamos interacciones novedosas entre algunos de los factores más importantes, como el aumento en la probabilidad del reclutamiento en la siguiente generación en especies con tasas mayores de producción de semillas, pero sólo cuando se emparejó con grandes cantidades de fundadores. Ya que las barreras más significativas para el éxito de la reubicación de plantas pueden superarse al mejorar las técnicas o resolver los temas a nivel de sitio por medio de un manejo y una intervención temprana, sugerimos que con la combinación del monitoreo a largo plazo con el manejo adaptativo los programas de reubicación pueden aumentar el prospecto de lograr el éxito a largo plazo.

Comparing demography inferred from age vs. stage in a perennial plant.

Life history theories analyze and predict variation in vital rates, such as survival and reproduction, based on age. The age-from-stage method to derive age-specific vital rates from stage data was developed because age-specific data are rarely obtained for plants. Age-specific vital rates derived by this method might underestimate effects of age on vital rates, because the models assume that vital rates do not vary within stage classes. Consequently, population models and life history summaries relying on these vital rates could be biased against detecting senescence. Here, we perform a comparative study of methods to estimate age-specific vital rates using monitoring data with known age and stage. We derived age-, stage-, and age-and-stage-specific vital rates with demographic data from a long-lived perennial, Silene spaldingii. Then, we derived three age-specific population matrix models (age, age-from-stage, and age-and-stage). For each model, we derived life history summaries commonly used in ecology: population growth rate, net reproductive value, relative reproductive values, stable age distribution, generation time, and sensitivity and elasticity of population growth rate. Many vital rates depended on both age and stage in S. spaldingii. However, this species does not senesce; in fact, the number of flowers increased with age. As expected, the age-from-stage method was not able to accurately recreate the age dependence in some life history summaries, such as relative reproductive value. The age-from-stage model suggested faster reproductive dynamics in S. spaldingii than the models based on known age, i.e., plants started to reproduce earlier, and fertility remained constant thereafter, which may lead to biased predictions about evolutionary consequences of age-dependent life history traits. However, population growth rate, generation time, and net reproductive rate did not differ significantly among the models. Our study demonstrated that some metrics are robust to imprecision in model structure, while others are more sensitive. In spite of these biases, this case study provides another example of the diversity of aging patterns in plants. Age can be essential information when studying senescence in plants, but demographic metrics that were not about age per se were similar across model structures.

Does masting scale with plant size? High reproductive variability and low synchrony in small and unproductive individuals.

BACKGROUND AND AIMS: In a range of plant species, the distribution of individual mean fecundity is skewed and dominated by a few highly fecund individuals. Larger plants produce greater seed crops, but the exact nature of the relationship between size and reproductive patterns is poorly understood. This is especially clear in plants that reproduce by exhibiting synchronized quasi-periodic variation in fruit production, a process called masting. METHODS: We investigated covariation of plant size and fecundity with individual-plant-level masting patterns and seed predation in 12 mast-seeding species: Pinus pinea, Astragalus scaphoides, Sorbus aucuparia, Quercus ilex, Q. humilis, Q. rubra, Q. alba, Q. montana, Chionochloa pallens, C. macra, Celmisia lyallii and Phormium tenax. KEY RESULTS: Fecundity was non-linearly related to masting patterns. Small and unproductive plants frequently failed to produce any seeds, which elevated their annual variation and decreased synchrony. Above a low fecundity threshold, plants had similar variability and synchrony, regardless of their size and productivity. CONCLUSIONS: Our study shows that within-species variation in masting patterns is correlated with variation in fecundity, which in turn is related to plant size. Low synchrony of low-fertility plants shows that the failure years were idiosyncratic to each small plant, which in turn implies that the small plants fail to reproduce because of plant-specific factors (e.g. internal resource limits). Thus, the behaviour of these sub-producers is apparently the result of trade-offs in resource allocation and environmental limits with which the small plants cannot cope. Plant size and especially fecundity and propensity for mast failure years play a major role in determining the variability and synchrony of reproduction in plants.

Arctic and boreal plant species decline at their southern range limits in the Rocky Mountains.

Climate change is predicted to cause a decline in warm-margin plant populations, but this hypothesis has rarely been tested. Understanding which species and habitats are most likely to be affected is critical for adaptive management and conservation. We monitored the density of 46 populations representing 28 species of arctic-alpine or boreal plants at the southern margin of their ranges in the Rocky Mountains of Montana, USA, between 1988 and 2014 and analysed population trends and relationships to phylogeny and habitat. Marginal populations declined overall during the past two decades; however, the mean trend for 18 dicot populations was -5.8% per year, but only -0.4% per year for the 28 populations of monocots and pteridophytes. Declines in the size of peripheral populations did not differ significantly among tundra, fen and forest habitats. Results of our study support predicted effects of climate change and suggest that vulnerability may depend on phylogeny or associated anatomical/physiological attributes.

Ability of matrix models to explain the past and predict the future of plant populations.

Uncertainty associated with ecological forecasts has long been recognized, but forecast accuracy is rarely quantified. We evaluated how well data on 82 populations of 20 species of plants spanning 3 continents explained and predicted plant population dynamics. We parameterized stage-based matrix models with demographic data from individually marked plants and determined how well these models forecast population sizes observed at least 5 years into the future. Simple demographic models forecasted population dynamics poorly; only 40% of observed population sizes fell within our forecasts' 95% confidence limits. However, these models explained population dynamics during the years in which data were collected; observed changes in population size during the data-collection period were strongly positively correlated with population growth rate. Thus, these models are at least a sound way to quantify population status. Poor forecasts were not associated with the number of individual plants or years of data. We tested whether vital rates were density dependent and found both positive and negative density dependence. However, density dependence was not associated with forecast error. Forecast error was significantly associated with environmental differences between the data collection and forecast periods. To forecast population fates, more detailed models, such as those that project how environments are likely to change and how these changes will affect population dynamics, may be needed. Such detailed models are not always feasible. Thus, it may be wiser to make risk-averse decisions than to expect precise forecasts from models.

Are dormant plants hedging their bets? Demographic consequences of prolonged dormancy in variable environments.

During the growing season, some individuals in perennial plant populations may remain alive belowground while others emerge. This phenomenon, known as prolonged dormancy, seems maladaptive, because prolonged dormancy delays growth and reproduction. However, prolonged dormancy may offer the benefit of safety while belowground, leading to the hypothesis that prolonged dormancy is a bet-hedging strategy. We evaluated this hypothesis using a 25-year demographic study of Astragalus scaphoides, an iteroparous perennial plant. First, we determined the relationship between prolonged dormancy and fitness using data from individuals in our population. This analysis showed that prolonged dormancy decreased arithmetic mean fitness and reduced variance in fitness. Geometric mean fitness was maximized at intermediate levels of prolonged dormancy. Empirical patterns of lifetime reproductive success confirm this relationship. We also compared fitness of plants in our population to hypothetical plants without prolonged dormancy, which generally revealed benefits of prolonged dormancy, even if plants could forgo prolonged dormancy without costs to other vital rates. Therefore, prolonged dormancy may indeed function as a bet-hedging strategy, but the benefits of remaining belowground outweigh the costs only for a subset of individuals. Bet hedging has been demonstrated in plants with simple life histories, such as annuals and monocarpic perennials; we present evidence that bet hedging may be important for plants with more complex life histories.

How do plant ecologists use matrix population models?

Matrix projection models are among the most widely used tools in plant ecology. However, the way in which plant ecologists use and interpret these models differs from the way in which they are presented in the broader academic literature. In contrast to calls from earlier reviews, most studies of plant populations are based on < 5 matrices and present simple metrics such as deterministic population growth rates. However, plant ecologists also cautioned against literal interpretation of model predictions. Although academic studies have emphasized testing quantitative model predictions, such forecasts are not the way in which plant ecologists find matrix models to be most useful. Improving forecasting ability would necessitate increased model complexity and longer studies. Therefore, in addition to longer term studies with better links to environmental drivers, priorities for research include critically evaluating relative/comparative uses of matrix models and asking how we can use many short-term studies to understand long-term population dynamics.

Pollen and water limitation in Astragalus scaphoides, a plant that flowers in alternate years.

Mast seeding is common in plant populations, but its causes have rarely been tested experimentally. We tested mechanisms of alternate-year flowering and fruit set in an iteroparous, bee-pollinated, herbaceous plant, Astragalus scaphoides, in semi-arid sagebrush steppe. Patterns of reproduction from 1986 to 1999 indicated that spring precipitation was a cue for synchronous flowering, and that increased pollination in high-flowering years was a fitness advantage of synchrony. We tested these patterns by adding supplemental water and pollen to plants in high- and low-flowering sites and years. Supplemental water had no effect on flowering or seed set, so water is not a proximate cue for reproduction, though it could be important over longer (>3 year) time scales. Supplemental pollination increased fruit set in low- but not high-flowering years, indicating that synchronous flowering increases pollination success. Many shorter-term studies also report increased fruit set after pollen supplementation, but not after resource addition. This pattern may reflect the fact that plants can store and reallocate resources, but not pollen, across multiple years. For animal-pollinated herbs such as these, uniting theories about pollination ecology and mast seeding may promote an understanding of the mechanisms that determine patterns of reproduction over time.

Rare plants are common where you find them.

Broad patterns in distribution and abundance can elucidate processes of evolution. A positive association between local abundance and the size of the geographic range has been demonstrated for closely related species across many taxa. This pattern is usually explained by assuming that species with smaller ranges are ecologically inferior (e.g., poor competitors or dispersers). Many areas of high endemism support local species that have evolved recently. The distribution of these neoendemics may reflect historical processes not accounted for by ecological, equilibrium hypotheses. We asked whether such traditional macroecological hypotheses also applied to the local abundance of seven narrowly endemic species and ecologically similar widespread congeners in the northern Rocky Mountains. For each of the 14 species, we estimated abundance of five randomly chosen populations by counting plants in 10 randomly located plots. The association between range size and local abundance was not positive. Instead, all seven narrow endemics were more abundant than their widespread congeners. Ecological specialization or differences in dispersal ability are not likely explanations for our results. We believe the local abundance of narrowly endemic species may be a sign of recent speciation. Most or all of our narrowly distributed species have probably not yet had time to spread to their full potential. Furthermore, theory predicts that speciation is more likely to occur in locally abundant populations. Our results suggest that strictly ecological mechanisms cannot explain abundance and distribution in regions with high neoendemism.

Empirical models of pollen limitation, resource acquisition, and mast seeding by a bee-pollinated wildflower.

Synchronous mast seeding is increasingly recognized as common in plant populations. Recent theoretical models show that synchronous mast seeding could be a consequence of resource allocation and storage within individual plants, coupled by pollen limitation in low-flowering years. We used long-term population and weather data to parameterize models of flowering based on stored resources and pollen limitation in Astragalus scaphoides, a bee-pollinated plant that flowers in alternate years. We used these models to test whether internal resource dynamics could explain mast seeding in A. scaphoides and, if so, whether synchrony was caused by pollen limitation and/or fluctuations in precipitation. We compared predictions of models that included all combinations of three factors: constant versus precipitation-dependent resource gain, uniform versus heterogeneous resource gain (among individual plants), and resource-dependent versus resource- and pollen-limited fruit set. Pollen limitation and heterogeneous resource gain were necessary and sufficient to explain alternate-year flowering, but precipitation increased the quantitative match between model predictions and flowering dynamics. Together, our results support the importance of density-dependent pollen limitation as an ultimate and proximate cause of mast seeding in A. scaphoides. Precipitation does not act as a direct cue for synchrony in this species but might affect long-term resource gain and fruiting dynamics.

Autecology of the Endangered Plant Howellia Aquatilis; Implications for Management and Reserve Design.

Howellia aquatilis is an annual aquatic plant of ephemeral ponds. It is considered extirpated or endangered throughout its range in the United States Pacific Northwest. I studied populations in the Swan Valley of Montana to determine life history traits and ecological attributed in order to influence planning decisions on lands managed for multiple use. Germination trials demonstrated that seeds of H. aquatilis require an aerobic environment and cool temperatures to germinate. Germination was highest with daily alternating temperatures and total darkness, and was unaffected by different light regime and aeration retreatment conditions of 50- and 100-d durations. Natural seed banks were largest immediately following seed dispersal and pond drawdown, but were reduced 82-90% by the following spring. Seeds remaining in the seed bank showed reduced germinability and vigor. Aquarium experiments indicate that growth of H. aquatilis is best in the peat substrate in which it occurs naturally, and is reduced by 45% in a more fine-textured organic soil and by 85% in a mineral soil. Multiple regression analyses of 12 environmental variables from 23 H. aquatilis ponds and comparisons between ponds with and without H. aquatilis suggest that pond depth, amount of dissolved solids in pond water, depth and composition of pond substrate, and degree of human-caused disturbance have significant effects on the abundance of H. aquatilis in the Swan Valley. Taken together, these results suggest that Howellia aquatilis is rare because it can persist in only a small subset of wetlands-freshwater ephemeral ponds with a shallow, coarse textured organic surface horizon. Thus, H. aquatilis will be sensitive to disturbances that alter pond water quality or substrate composition. Lack of a persistent seed bank makes H. aquatilis prone to large fluctuations in population size due to environmental fluctuations. Both habitat specificity and large variations in population size are often associated with a high risk of extinction. Howellia aquatilis can only persist during periods of climatic fluctuation as a metapopulation in an area that contains large numbers of appropriate ponds of various depths. Consequently, long-term protection of this rare species will require habitat protection in large wetland complexes throughout its range.