Global change impacts on cacti (Cactaceae): current threats, challenges and conservation solutions.

BACKGROUND: The plant family Cactaceae provides some of the most striking examples of adaptive evolution, expressing undeniably the most spectacular New World radiation of succulent plants distributed across arid and semi-arid regions of the Americas. Cacti are widely regarded for their cultural, economic and ecological value, yet they are also recognized as one of the most threatened and endangered taxonomic groups on the planet. SCOPE: This paper reviews current threats to species of cacti that have distributions in arid to semi-arid subtropical regions. Our review focuses primarily on four global change forces: (1) increases in atmospheric CO2 concentrations; (2) increases in mean annual temperatures and heat waves; (3) increases in the duration, frequency and intensity of droughts; and (4) and increases in competition and wildfire frequency from invasion by non-native species. We provide a broad range of potential priorities and solutions for stemming the extinction risk of cacti species and populations. CONCLUSIONS: Mitigating ongoing and emerging threats to cacti will require not only strong policy initiatives and international cooperation, but also new and creative approaches to conservation. These approaches include determining species at risk from climate extremes, enhancing habitat quality after disturbance, approaches and opportunities for ex situ conservation and restoration, and the potential use of forensic tools for identifying plants that have been removed illegally from the wild and sold on open markets.

Heritability and variance components of seed size in wild species: influences of breeding design and the number of genotypes tested.

Seed size affects individual fitness in wild plant populations, but its ability to evolve may be limited by low narrow-sense heritability (h2). h2 is estimated as the proportion of total phenotypic variance (σ2P) attributable to additive genetic variance (σ2A), so low values of h2 may be due to low σ2A (potentially eroded by natural selection) or to high values of the other factors that contribute to σ2P, such as extranuclear maternal effects (m2) and environmental variance effects (e2). Here, we reviewed the published literature and performed a meta-analysis to determine whether h2 of seed size is routinely low in wild populations and, if so, which components of σ2P contribute most strongly to total phenotypic variance. We analyzed available estimates of narrow-sense heritability (h2) of seed size, as well as the variance components contributing to these parameters. Maternal and environmental components of σ2P were significantly greater than σ2A, dominance, paternal, and epistatic components. These results suggest that low h2 of seed size in wild populations (the mean value observed in this study was 0.13) is due to both high values of maternally derived and environmental (residual) σ2, and low values of σ2A in seed size. The type of breeding design used to estimate h2 and m2 also influenced their values, with studies using diallel designs generating lower variance ratios than nested and other designs. e2 was not influenced by breeding design. For some breeding designs, the number of genotypes included in a study also influenced the resulting h2 and e2 estimates, but not m2. Our data support the view that a diallel design is better suited than the alternatives for the accurate estimation of σ2A in seed size due to its factorial design and the inclusion of reciprocal crosses, which allows the independent estimation of both additive and non-additive components of variance.

Genotype × environment interaction obscures genetic sources of variation in seed size in Dithyrea californica but provides the opportunity for selection on phenotypic plasticity.

PREMISE: In many species, seed size influences individual fitness, but its heritability is low, impeding its evolution. In heterogeneous environments, even if heritability of seed size is low, genetic variation in phenotypic plasticity for seed size may provide the opportunity for selection, but this possibility has rarely been investigated in wild species. The evolutionary trajectory of seed size depends on whether additive, maternal, or non-additive genetic variance dominates; moreover, the expression of any of these sources of variance may be environment-dependent, reflecting genetic variation in plasticity. In this study, we examined these sources of variation in seed size and their response to drought in Dithyrea californica. METHODS: We used a diallel design to estimate variance components for seed size in three greenhouse-raised populations sampled from California and northern Mexico. We replicated diallels in two watering treatments to examine genetic parameters and genotype × environment interactions affecting seed size. We estimated general (GCA) and specific (SCA) combining ability, reciprocal effects (RGCA and RSCA), and their interactions with water availability, and we sought evidence that sexual conflict influences seed size. RESULTS: Norms of reaction revealed genetic variation in plasticity for seed size in each population. Seed size in D. californica is determined by the combination of watering treatment, GCA and RGCA; parental identity and water availability do not consistently affect seed size, and we detected no evidence for sexual conflict. CONCLUSIONS: Multiple sources of genetic variation in phenotypic plasticity for seed size have the potential to influence its evolutionary trajectory in heterogenous environments.

What determines the evolutionary trajectories of wild plant species? Approaches to the study of quantitative fitness-related traits.

Wild plant species provide excellent examples of qualitative traits that evolve in response to environmental challenges (e.g., flower color, heavy metal tolerance, cyanogenesis, and male sterility). In addition to such discrete characters, a dazzling array of continuously distributed, quantitative traits are expressed at every phase of the life cycle. These traits are known or suspected to have evolved by natural selection because they are heritable, differ among populations or closely related taxa occupying distinct habitats, and have individual phenotypes associated with survival and reproductive success. This special issue [American Journal of Botany 109(11)] focuses on the tools and approaches for detecting or inferring the ecological and genetic factors contributing to changes in genetically based variation of quantitative traits within or among populations, or causing their divergence among taxa. The assembled articles use one or more of three primary approaches to detect the process or outcome of natural selection on morphological, life history, reproductive, chemical, and physiological quantitative traits: the analysis of phenotypic or artificially imposed selection to detect direct and indirect selection on traits whose function is well-understood; common garden experiments, including reciprocal transplants and "resurrection" experiments; and quantitative genetic analyses designed to detect and to estimate the environmental and genetic sources of phenotypic variation or to forecast short-term evolutionary change. Together, these articles examine and reveal the adaptive capacity of quantitative traits and the genetically based constraints that may limit their directional evolutionary change, thereby informing and testing inferences, hypotheses, and predictions concerning the evolutionary trajectories of wild plant species.

Episodic recruitment in the saguaro cactus is driven by multidecadal periodicities.

Each year, an individual mature large saguaro cactus produces about one million seeds in attractive juicy fruits that lure seed predators and seed dispersers to a 3-month feast. From the million seeds produced, however, only a few will persist into mature saguaros. A century of research on saguaro population dynamics has led to the conclusion that saguaro recruitment is an episodic event that depends on the convergence of suitable conditions for survival during the critical early stages. Because most data have been collected in Arizona, particularly in the surroundings of Tucson, most research has relied on a limited amount of environmental variation. In this study, we upscaled this knowledge on saguaro recruitment to a regional scale with a new method that used the inverse-growth modeling of 1,487 saguaros belonging to 13 populations in a latitudinal gradient ranging from arid desert to tropical thornscrub forest in Sonora, Mexico. Using generalized linear and additive mixed models, we created two 110-yr-long saguaro recruitment curves: one driven only by previous size, and the second driven by size, drought, and soil structure. We found evidence that saguaro recruitment is indeed episodic, with periodicities of 20-30 yr, possibly related to strong El Niño Southern Oscillation events. Our results suggest that saguaros rely on multidecadal periodic pulses of good beneficial years to incorporate new individuals into their populations. Inverse-growth modeling can be used in a wide variety of plant species to study their recruitment dynamics.

Population projections of an endangered cactus suggest little impact of climate change.

Population projections coupled with downscaled climate projections are a powerful tool that allows predicting future population dynamics of vulnerable plants in the face of a changing climate. Traditional approaches used to predict the vulnerability of plants to climate change (e.g. species distribution models) fail to mechanistically describe the basis of a population's dynamics and thus cannot be expected to correctly predict its temporal trends. In this study, we used a 23-year demographic dataset of the acuña cactus, an endangered species, to predict its population dynamics to the end of the century. We used integral projection models to describe its vital rates and population dynamics in relation to plant volume and key climatic variables. We used the resulting climate-driven IPM along with climatic projections to predict the population growth rates from 1991 to 2099. We found the average population growth rate of this population between 1991 and 2013 to be 0.70 (95% CI 0.61-0.79). This result confirms that the population of acuña cactus has been declining and that this decline is due to demographic structure and climate conditions. However, the projection model also predicts that, up to 2080, the population will remain relatively stable mainly due to the survival of its existing adult individuals. Notwithstanding, the long-term viability of the populations can only be achieved through the recruitment of new individuals.

Nonlinear modeling of saguaro growth rates reveals the importance of temperature for size-dependent growth.

PREMISE: The saguaro cactus is an iconic species of the Sonoran Desert. Its individual growth rates have been investigated for over 100 years. Its growth dynamics have been studied using phenomenological models intended to estimate growth, but not to understand the underlying biological processes. Most studies have suggested summer rainfall as the sole factor determining saguaro growth, overlooking the influence of other factors related to the process of growth. METHODS: We analyzed the annual growth rates for 13 saguaro populations in the Sonoran Desert using nonlinear models. These are better suited to analyze growth since they consider the fact that maximum growth rates diminish just before the onset of reproduction. We related model parameters to the local climate. RESULTS: The most parsimonious model was the Ricker function that described growth considering cactus decline with age. Variance in temperature, rather than precipitation, was more closely related to growth. Higher variance in temperature at the beginning of the warm season was detrimental to saguaro growth. CONCLUSIONS: Simple nonlinear equations modeled growth rate using biologically interpretable parameters related to climate factors. Because the temperature is projected to increase in both mean and variance by climate change, the population dynamics of this iconic cactus are likely to be affected.

Maternal adjustment of offspring provisioning and the consequences for dispersal.

Phenotypic plasticity in seed provisioning is a widespread phenomenon in plant populations that is often manifested as environmentally induced maternal effects. Environmental maternal effects can be beneficial if they influence population dynamic functions of seeds in a way that increases fitness, such as escaping from crowding. Using the winter annual plant, Dithyrea californica, we studied the response of seed provisioning to the maternal competitive environment and the associated seed dispersal consequences. We measured the average size of seeds produced by plants experiencing different competitive environments in order to test the hypothesis that mother plants respond to crowding by providing fewer resources to each offspring. We also hypothesized that smaller seeds produced by crowded mothers would benefit from greater dispersal away from their high-density natal habitat. We marked seeds with fluorescent paint while still attached to the mother plant, recorded seed diameter, and followed them for nine months after dispersal, recording the distance they moved from the mother plant. Plants that experienced more competition produced smaller seeds that dispersed farther from their mother plant. Larger seed diameter was previously shown to be'associated with greater competitive ability in D. californica. Thus the production of smaller seeds in more competitive environments implies a possible trade-off between competitive ability and dispersal arising from an environmentally driven aspect of phenotype. Fitness consequences of this trade-off in the context of the year-to-year variation in rainfall and density are uncertain.