Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

Host phenology regulates parasite–host demographic cycles and eco‐evolutionary feedbacks

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.     

Influence of environmental conditions at spawning sites and migration routes on adaptive variation and population connectivity in Chinook salmon

Many species that undergo long breeding migrations, such as anadromous fishes, face highly heterogeneous environments along their migration corridors and at their spawning sites. These environmental challenges encountered at different life stages may act as strong selective pressures and drive local adaptation. However, the relative influence of environmental conditions along the migration corridor compared with the conditions at spawning sites on driving selection is still unknown. In this study, we performed genome–environment associations (GEA) to understand the relationship between landscape and environmental conditions driving selection in seven populations of the anadromous Chinook salmon (Oncorhynchus tshawytscha)—a species of important economic, social, cultural, and ecological value—in the Columbia River basin. We extracted environmental variables for the shared migration corridors and at distinct spawning sites for each population, and used a Pool‐seq approach to perform whole genome resequencing. Bayesian and univariate GEA tests with migration‐specific and spawning site‐specific environmental variables indicated many more candidate SNPs associated with environmental conditions at the migration corridor compared with spawning sites. Specifically, temperature, precipitation, terrain roughness, and elevation variables of the migration corridor were the most significant drivers of environmental selection. Additional analyses of neutral loci revealed two distinct clusters representing populations from different geographic regions of the drainage that also exhibit differences in adult migration timing (summer vs. fall). Tests for genomic regions under selection revealed a strong peak on chromosome 28, corresponding to the GREB1L/ROCK1 region that has been identified previously in salmonids as a region associated with adult migration timing. Our results show that environmental variation experienced throughout migration corridors imposed a greater selective pressure on Chinook salmon than environmental conditions at spawning sites.     

Coinfection with a virus constrains within‐host infection load but increases transmission potential of a highly virulent fungal plant pathogen

The trade‐off between within‐host infection rate and transmission to new hosts is predicted to constrain pathogen evolution, and to maintain polymorphism in pathogen populations. Pathogen life‐history stages and their correlations that underpin infection development may change under coinfection with other parasites as they compete for the same limited host resources. Cross‐kingdom interactions are common among pathogens in both natural and cultivated systems, yet their impacts on disease ecology and evolution are rarely studied. The host plant Plantago lanceolata is naturally infected by both Phomopsis subordinaria, a seed killing fungus, as well as Plantago lanceolata latent virus (PlLV) in the Åland Islands, SW Finland. We performed an inoculation assay to test whether coinfection with PlLV affects performance of two P. subordinaria strains, and the correlation between within‐host infection rate and transmission potential. The strains differed in the measured life‐history traits and their correlations. Moreover, we found that under virus coinfection, within‐host infection rate of P. subordinaria was smaller but transmission potential was higher compared to strains under single infection. The negative correlation between within‐host infection rate and transmission potential detected under single infection became positive under coinfection with PlLV. To understand whether within‐host and between‐host dynamics are correlated in wild populations, we surveyed 260 natural populations of P. lanceolata for P. subordinaria infection occurrence. When infections were found, we estimated between‐hosts dynamics by determining pathogen population size as the proportion of infected individuals, and within‐host dynamics by counting the proportion of infected flower stalks in 10 infected plants. In wild populations, the proportion of infected flower stalks was positively associated with pathogen population size. Jointly, our results suggest that the trade‐off between within‐host infection load and transmission may be strain specific, and that the pathogen life‐history that underpin epidemics may change depending on the diversity of infection, generating variation in disease dynamics.     

Age is not just a number—Mathematical model suggests senescence affects how fish populations respond to different fishing regimes

Senescence is often described as an age‐dependent increase in natural mortality (known as actuarial senescence) and an age‐dependent decrease in fecundity (known as reproductive senescence), and its role in nature is still poorly understood. Based on empirical estimates of reproductive and actuarial senescence, we used mathematical simulations to explore how senescence affects the population dynamics of Coregonus albula, a small, schooling salmonid fish. Using an empirically based eco‐evolutionary model, we investigated how the presence or absence of senescence affects the eco‐evolutionary dynamics of a fish population during pristine, intensive harvest, and recovery phases. Our simulation results showed that the presence or absence of senescence affected how the population responded to the selection regime. At an individual level, gillnetting caused a larger decline in asymptotic length when senescence was present, compared to the nonsenescent population, and the opposite occurred when fishing was done by trawling. This change was accompanied by evolution toward younger age at maturity. At the population level, the change in biomass and number of fish in response to different fishery size‐selection patterns depended on the presence or absence of senescence. Since most life‐history and fisheries models ignore senescence, they may be over‐estimating reproductive capacity and under‐estimating natural mortality. Our results highlight the need to understand the combined effects of life‐history characters such as senescence and fisheries selection regime to ensure the successful management of our natural resources.     

Spatial and environmental effects on Coho Salmon life history trait variation

Adult size, egg size, fecundity, and mass of gonads are affected by trade‐offs between reproductive investment and environmental conditions shaping the evolution of life history traits among populations for widely distributed species. Coho salmon Oncorhynchus kisutch have a large geographic distribution, and different environmental conditions are experienced by populations throughout their range. We examined the effect of environmental variables on female size, egg size, fecundity, and reproductive investment of populations of Coho Salmon from across British Columbia using an information theoretic approach. Female size increased with latitude and decreased with migration distance from the ocean to spawning locations. Egg size was lowest for intermediate intragravel temperature during incubation, decreased with migration distance, but increased in rivers below lakes. Fecundity increased with latitude, warmer temperature during the spawning period, and river size, but decreased in rivers below lakes compared with rivers with tributary sources. Relative gonad size increased with latitude and decreased with migration distance. Latitude of spawning grounds, migratory distance, and temperatures experienced by a population, but also hydrologic features—river size and headwater source—are influential in shaping patterns of reproductive investment, particularly egg size. Although, relative gonad size varied with latitude and migration distance, how gonadal mass was partitioned gives insight into the trade‐off between egg size and fecundity. The lack of an effect of latitude on egg size suggests that local optima for egg size related to intragravel temperature may drive the variation in fecundity observed among years.     

gauseR: Simple methods for fitting Lotka‐Volterra models describing Gause’s “Struggle for Existence”

Point 1: The ecological models of Alfred J. Lotka and Vito Volterra have had an enormous impact on ecology over the past century. Some of the earliest—and clearest—experimental tests of these models were famously conducted by Georgy Gause in the 1930s. Although well known, the data from these experiments are not widely available and are often difficult to analyze using standard statistical and computational tools.Point 2: Here, we introduce the gauseR package, a collection of tools for fitting Lotka‐Volterra models to time series data of one or more species. The package includes several methods for parameter estimation and optimization, and includes 42 datasets from Gause''s species interaction experiments and related work. Additionally, we include with this paper a short blog post discussing the historical importance of these data and models, and an R vignette with a walk‐through introducing the package methods. The package is available for download at github.com/adamtclark/gauseR.Point 3: To demonstrate the package, we apply it to several classic experimental studies from Gause, as well as two other well‐known datasets on multi‐trophic dynamics on Isle Royale, and in spatially structured mite populations. In almost all cases, models fit observations closely and fitted parameter values make ecological sense.Point 4: Taken together, we hope that the methods, data, and analyses that we present here provide a simple and user‐friendly way to interact with complex ecological data. We are optimistic that these methods will be especially useful to students and educators who are studying ecological dynamics, as well as researchers who would like a fast tool for basic analyses.     

Old males reduce melanin‐pigmented traits and increase reproductive outcome under worse environmental conditions in common kestrels

Secondary sexual traits displayed by males and females may have evolved as a signal of individual quality. However, both individual quality and investment on producing or maintaining enhanced sexual traits change as individuals age. At the same time, the costs associated to produce sexual traits might be attenuated or increased if environmental conditions are benign or worse respectively. Accordingly, environmental conditions are expected to shape the association between the expression of sexual traits and their reproductive outcome as individuals age. Nonetheless, little is known about the environmental influence on the co‐variation between sexual traits and reproductive outcome throughout the life of individuals. We studied the age‐dependency of the number and size of back spots, a melanin‐based and sexual trait in adults of common kestrels (Falco tinnunculus). We analysed the age‐dependence of reproductive traits and the environmental influence, defined as vole abundance, using a 10‐year individual‐based dataset. We broke down age‐related changes of reproductive traits into within‐ and between‐individual variation to assess their contribution to population‐level patterns. Our results showed a within‐individual decrease in the number, but not the size, of back spots in males. The size of back spots was positively correlated with food availability in males. Reproductive performance of males increased as they aged, in agreement with the life‐history theory but depending of vole abundance. Remarkably, we found that having fewer back spots was positively associated with clutch size only for old individuals under low‐food conditions. We suggest that environmental variation may shape the association between the expression of a sexual signal and reproductive outcome. We speculate that the reliability of sexual traits is higher when environmental conditions are poor only for old individuals. Within an evolutionary context, we suggest that the expression of sexual traits might be constrained by environmental conditions at later stages of life.     

The effect of dilution on eco‐evolutionary dynamics of experimental microbial communities

Changing environmental conditions can infer structural modifications of predator‐prey communities. New conditions often increase mortality which reduces population sizes. Following this, predation pressure may decrease until populations are dense again. Dilution may thus have substantial impact not only on ecological but also on evolutionary dynamics because it amends population densities. Experimental studies, in which microbial populations are maintained by a repeated dilution into fresh conditions after a certain period, are extensively used approaches allowing us to obtain mechanistic insights into fundamental processes. By design, dilution, which depends on transfer volume (modifying mortality) and transfer interval (determining the time of interaction), is an inherent feature of these experiments, but often receives little attention. We further explore previously published data from a live predator‐prey (bacteria and ciliates) system which investigated eco‐evolutionary principles and apply a mathematical model to predict how various transfer volumes and transfer intervals would affect such an experiment. We find not only the ecological dynamics to be modified by both factors but also the evolutionary rates to be affected. Our work predicts that the evolution of the anti‐predator defense in the bacteria, and the evolution of the predation efficiency in the ciliates, both slow down with lower transfer volume, but speed up with longer transfer intervals. Our results provide testable hypotheses for future studies of predator‐prey systems, and we hope this work will help improve our understanding of how ecological and evolutionary processes together shape composition of microbial communities.     

Is the grass always greener? Land surface phenology reveals differences in peak and season‐long vegetation productivity responses to climate and management

Vegetation phenology—the seasonal timing and duration of vegetative phases—is controlled by spatiotemporally variable contributions of climatic and environmental factors plus additional potential influence from human management. We used land surface phenology derived from the Advanced Very High Resolution Radiometer and climate data to examine variability in vegetation productivity and phenological dates from 1989 to 2014 in the U.S. Northwestern Plains, a region with notable spatial heterogeneity in climate, vegetation, and land use. We first analyzed interannual trends in six phenological measures as a baseline. We then demonstrated how including annual‐resolution predictors can provide more nuanced insights into measures of phenology between plant communities and across the ecoregion. Across the study area, higher annual precipitation increased both peak and season‐long productivity. In contrast, higher mean annual temperatures tended to increase peak productivity but for the majority of the study area decreased season‐long productivity. Annual precipitation and temperature had strong explanatory power for productivity‐related phenology measures but predicted date‐based measures poorly. We found that relationships between climate and phenology varied across the region and among plant communities and that factors such as recovery from disturbance and anthropogenic management also contributed in certain regions. In sum, phenological measures did not respond ubiquitously nor covary in their responses. Nonclimatic dynamics can decouple phenology from climate; therefore, analyses including only interannual trends should not assume climate alone drives patterns. For example, models of areas exhibiting greening or browning should account for climate, anthropogenic influence, and natural disturbances. Investigating multiple aspects of phenology to describe growing‐season dynamics provides a richer understanding of spatiotemporal patterns that can be used for predicting ecosystem responses to future climates and land‐use change. Such understanding allows for clearer interpretation of results for conservation, wildlife, and land management.     

Gillespie eco‐evolutionary models (GEMs) reveal the role of heritable trait variation in eco‐evolutionary dynamics

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco‐evolutionary models usually fail to track how variation changes through time. Moreover, eco‐evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco‐evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco‐evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm – an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig–MacArthur consumer–resource model. We show not only how heritable trait variation fuels trait evolution and influences eco‐evolutionary dynamics, but also how the erosion of variation through time may hinder eco‐evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco‐evolutionary and evolutionary modeling by removing long‐standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco‐evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.     

Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?

Reproductive isolation in response to divergent selection is often mediated via third‐party interactions. Under these conditions, speciation is inextricably linked to ecological context. We present a novel framework for understanding arthropod speciation as mediated by Wolbachia, a microbial endosymbiont capable of causing host cytoplasmic incompatibility (CI). We predict that sympatric host sister‐species harbor paraphyletic Wolbachia strains that provide CI, while well‐defined congeners in ecological contact and recently diverged noninteracting congeners are uninfected due to Wolbachia redundancy. We argue that Wolbachia provides an adaptive advantage when coupled with reduced hybrid fitness, facilitating assortative mating between co‐occurring divergent phenotypes—the contact contingency hypothesis. To test this, we applied a predictive algorithm to empirical pollinating fig wasp data, achieving up to 91.60% accuracy. We further postulate that observed temporal decay of Wolbachia incidence results from adaptive host purging—adaptive decay hypothesis—but implementation failed to predict systematic patterns. We then account for post‐zygotic offspring mortality during CI mating, modeling fitness clines across developmental resources—the fecundity trade‐off hypothesis. This model regularly favored CI despite fecundity losses. We demonstrate that a rules‐based algorithm accurately predicts Wolbachia infection status. This has implications among other systems where closely related sympatric species encounter adaptive disadvantage through hybridization.     

Male‐biased dispersal in a fungus‐gardening ant symbiosis

For nearly all organisms, dispersal is a fundamental life‐history trait that can shape their ecology and evolution. Variation in dispersal capabilities within a species exists and can influence population genetic structure and ecological interactions. In fungus‐gardening (attine) ants, co‐dispersal of ants and mutualistic fungi is crucial to the success of this obligate symbiosis. Female‐biased dispersal (and gene flow) may be favored in attines because virgin queens carry the responsibility of dispersing the fungi, but a paucity of research has made this conclusion difficult. Here, we investigate dispersal of the fungus‐gardening ant Trachymyrmex septentrionalis using a combination of maternally (mitochondrial DNA) and biparentally inherited (microsatellites) markers. We found three distinct, spatially isolated mitochondrial DNA haplotypes; two were found in the Florida panhandle and the other in the Florida peninsula. In contrast, biparental markers illustrated significant gene flow across this region and minimal spatial structure. The differential patterns uncovered from mitochondrial DNA and microsatellite markers suggest that most long‐distance ant dispersal is male‐biased and that females (and concomitantly the fungus) have more limited dispersal capabilities. Consequently, the limited female dispersal is likely an important bottleneck for the fungal symbiont. This bottleneck could slow fungal genetic diversification, which has significant implications for both ant hosts and fungal symbionts regarding population genetics, species distributions, adaptive responses to environmental change, and coevolutionary patterns.     

The effects of adaptation to urea on feeding rates and growth in Drosophila larvae

A collection of forty populations were used to study the phenotypic adaptation of Drosophila melanogaster larvae to urea‐laced food. A long‐term goal of this research is to map genes responsible for these phenotypes. This mapping requires large numbers of populations. Thus, we studied fifteen populations subjected to direct selection for urea tolerance and five controls. In addition, we studied another twenty populations which had not been exposed to urea but were subjected to stress or demographic selection. In this study, we describe the differentiation in these population for six phenotypes: (1) larval feeding rates, (2) larval viability in urea‐laced food, (3) larval development time in urea‐laced food, (4) adult starvation times, (5) adult desiccation times, and (6) larval growth rates. No significant differences were observed for desiccation resistance. The demographically/stress‐selected populations had longer times to starvation than urea‐selected populations. The urea‐adapted populations showed elevated survival and reduced development time in urea‐laced food relative to the control and nonadapted populations. The urea‐adapted populations also showed reduced larval feeding rates relative to controls. We show that there is a strong linear relationship between feeding rates and growth rates at the same larval ages feeding rates were measured. This suggests that feeding rates are correlated with food intake and growth. This relationship between larval feeding rates, food consumption, and efficiency has been postulated to involve important trade‐offs that govern larval evolution in stressful environments. Our results support the idea that energy allocation is a central organizing theme in adaptive evolution.     

Multigenerational exposure to increased temperature reduces metabolic rate but increases boldness in Gambusia affinis

Acute exposure to warming temperatures increases minimum energetic requirements in ectotherms. However, over and within multiple generations, increased temperatures may cause plastic and evolved changes that modify the temperature sensitivity of energy demand and alter individual behaviors. Here, we aimed to test whether populations recently exposed to geothermally elevated temperatures express an altered temperature sensitivity of metabolism and behavior. We expected that long‐term exposure to warming would moderate metabolic rate, reducing the temperature sensitivity of metabolism, with concomitant reductions in boldness and activity. We compared the temperature sensitivity of metabolic rate (acclimation at 20 vs. 30°C) and allometric slopes of routine, standard, and maximum metabolic rates, in addition to boldness and activity behaviors, across eight recently divergent populations of a widespread fish species (Gambusia affinis). Our data reveal that warm‐source populations express a reduced temperature sensitivity of metabolism, with relatively high metabolic rates at cool acclimation temperatures and relatively low metabolic rates at warm acclimation temperatures compared to ambient‐source populations. Allometric scaling of metabolism did not differ with thermal history. Across individuals from all populations combined, higher metabolic rates were associated with higher activity rates at 20°C and bolder behavior at 30°C. However, warm‐source populations displayed relatively bolder behavior at both acclimation temperatures compared to ambient‐source populations, despite their relatively low metabolic rates at warm acclimation temperatures. Overall, our data suggest that in response to warming, multigenerational exposure (e.g., plasticity, adaptation) may not result in trait change directed along a simple “pace‐of‐life syndrome” axis, instead causing relative decreases in metabolism and increases in boldness. Ultimately, our data suggest that multigenerational warming may produce a novel combination of physiological and behavioral traits, with consequences for animal performance in a warming world.     

Dynamics of bird assemblages in response to temporally and spatially variable resources in arid Australia

Bird assemblages in arid Australia are often characterized as being highly variable through time in response to boom and bust dynamics, although the importance of habitat in structuring assemblages at a local‐scale is also recognized. We use a novel approach to investigate the importance of rainfall variability in structuring bird assemblages in a resource‐limited environment. Monthly bird surveys were conducted at ten plots for 8 years at a botanical and zoological park in central Australia, including five irrigated plots within a fenced area and five natural plots outside. Irrigation—used to promote growth, flowering, and fruiting of plants—created an artificial resource‐enhanced environment against which the response of birds to natural fluctuations in season and rainfall were compared. Species richness was generally maintained at a higher level in resource‐enhanced plots during dry times but was higher in natural plots when rainfall was high, mainly due to increases in granivores and insectivores. Honeyeaters were consistently more abundant at irrigated plots. Rainfall was important in structuring bird assemblages at all plots; however, assemblages were more stable in irrigated plots and did not respond as dramatically to a period of very high rainfall. The comparative smoothing of fluctuations in the composition and abundance of birds in irrigated areas highlights the importance of primary productivity, normally tied to rainfall, in driving temporal change in arid‐zone bird communities. There was also evidence that different plots in differing habitats supported distinct bird assemblages and that this spatial distinctiveness persisted irrespective of rainfall and determined, to some extent, the response to rainfall. Our study is one of few long‐term studies of arid bird assemblages and highlights the importance of both long‐term cycles of productivity driven by rain and season as well as site differences in the dynamics of arid‐zone bird communities. These insights are particularly valuable as climate change further exacerbates rainfall variability worldwide and initiatives to conserve avifauna in increasingly extreme environments may be required.     

Demographic history and local adaptation of Myripnois dioica (Asteraceae) provide insight on plant evolution in northern China flora

The flora of northern China forms the main part of the Sino‐Japanese floristic region and is located in a south–north vegetative transect in East Asia. Phylogeographic studies have demonstrated that an arid belt in this region has promoted divergence of plants in East Asia. However, little is known about how plants that are restricted to the arid belt of flora in northern China respond to climatic oscillation and environmental change. Here, we used genomic‐level data of Myripnois dioica across its distribution as a representative of northern China flora to reconstruct plant demographic history, examine local adaptation related to environmental disequilibrium, and investigate the factors related to effective population size change. Our results indicate M. dioica originated from the northern area and expanded to the southern area, with the Taihang Mountains serving as a physical barrier promoting population divergence. Genome‐wide evidence found strong correlation between genomic variation and environmental factors, specifically signatures associated with local adaptation to drought stress in heterogeneous environments. Multiple linear regression analyses revealed joint effects of population age, mean temperature of coldest quarter, and precipitation of wettest month on effective population size (Ne). Our current study uses M. dioica as a case for providing new insights into the evolutionary history and local adaptation of northern China flora and provides qualitative strategies for plant conservation.