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.

Release from herbivory does not confer invasion success for Eugenia uniflora in Florida.

One of the most commonly cited hypotheses explaining invasion success is the enemy release hypothesis (ERH), which maintains that populations are regulated by coevolved natural enemies where they are native but are relieved of this pressure in the new range. However, the role of resident enemies in plant invasion remains unresolved. We conducted a field experiment to test predictions of the ERH empirically using a system of native, introduced invasive, and introduced non-invasive Eugenia congeners in south Florida. Such experiments are rarely undertaken but are particularly informative in tests of the ERH, as they simultaneously identify factors allowing invasive species to replace natives and traits determining why most introduced species are unsuccessful invaders. We excluded insect herbivores from seedlings of Eugenia congeners where the native and invasive Eugenia co-occur, and compared how herbivore exclusion affected foliar damage, growth, and survival. We found no evidence to support the ERH in this system, instead finding that the invasive E. uniflora sustained significantly more damage than the native and introduced species. Interestingly, E. uniflora performed better than, or as well as, its congeners in terms of growth and survival, in spite of higher damage incidence. Further, although herbivore exclusion positively influenced Eugenia seedling survival, there were few differences among species and no patterns in regard to invasion status or origin. We conclude that the ability of E. uniflora to outperform its native and introduced non-invasive congeners, and not release from insect herbivores, contributes to its success as an invader in Florida.

Direct and legacy effects of long-term elevated CO2 on fine root growth and plant-insect interactions.

Increasing atmospheric CO2 concentrations alter leaf physiology, with effects that cascade to communities and ecosystems. Yet, responses over cycles of disturbance and recovery are not well known, because most experiments span limited ecological time. We examined the effects of CO2 on root growth, herbivory and arthropod biodiversity in a woodland from 1996 to 2006, and the legacy of CO2 enrichment on these processes during the year after the CO2 treatment ceased. We used minirhizotrons to study root growth, leaf censuses to study herbivory and pitfall traps to determine the effects of elevated CO2 on arthropod biodiversity. Elevated CO2 increased fine root biomass, but decreased foliar nitrogen and herbivory on all plant species. Insect biodiversity was unchanged in elevated CO2. Legacy effects of elevated CO2 disappeared quickly as fine root growth, foliar nitrogen and herbivory levels recovered in the next growing season following the cessation of elevated CO2. Although the effects of elevated CO2 cascade through plants to herbivores, they do not reach other trophic levels, and biodiversity remains unchanged. The legacy of 10 yr of elevated CO2 on plant-herbivore interactions in this system appear to be minimal, indicating that the effects of elevated CO2 may not accumulate over cycles of disturbance and recovery.

Fire, hurricane and carbon dioxide: effects on net primary production of a subtropical woodland.

Disturbance affects most terrestrial ecosystems and has the potential to shape their responses to chronic environmental change. Scrub-oak vegetation regenerating from fire disturbance in subtropical Florida was exposed to experimentally elevated carbon dioxide (CO2) concentration (+350 µl l(-1)) using open-top chambers for 11 yr, punctuated by hurricane disturbance in year 8. Here, we report the effects of elevated CO2 on aboveground and belowground net primary productivity (NPP) and nitrogen (N) cycling during this experiment. The stimulation of NPP and N uptake by elevated CO2 peaked within 2 yr after disturbance by fire and hurricane, when soil nutrient availability was high. The stimulation subsequently declined and disappeared, coincident with low soil nutrient availability and with a CO2 -induced reduction in the N concentration of oak stems. These findings show that strong growth responses to elevated CO2 can be transient, are consistent with a progressively limited response to elevated CO2 interrupted by disturbance, and illustrate the importance of biogeochemical responses to extreme events in modulating ecosystem responses to global environmental change.

Herbivory by an introduced Asian weevil negatively affects population growth of an invasive Brazilian shrub in Florida.

The enemy release hypothesis (ERH) is often cited to explain why some plants successfully invade natural communities while others do not. This hypothesis maintains that plant populations are regulated by coevolved enemies in their native range but are relieved of this pressure where their enemies have not been co-introduced. Some studies have shown that invasive plants sustain lower levels of herbivore damage when compared to native species, but how damage affects fitness and population dynamics remains unclear. We used a system of co-occurring native and invasive Eugenia congeners in south Florida (USA) to experimentally test the ERH, addressing deficiencies in our understanding of the role of natural enemies in plant invasion at the population level. Insecticide was used to experimentally exclude insect herbivores from invasive Eugenia uniflora and its native co-occurring congeners in the field for two years. Herbivore damage, plant growth, survival, and population growth rates for the three species were then compared for control and insecticide-treated plants. Our results contradict the ERH, indicating that E. uniflora sustains more herbivore damage than its native congeners and that this damage negatively impacts stem height, survival, and population growth. In addition, most damage to E. uniflora, a native of Brazil, is carried out by Myllocerus undatus, a recently introduced weevil from Sri Lanka, and M. undatus attacks a significantly greater proportion of E. uniflora leaves than those of its native congeners. This interaction is particularly interesting because M. undatus and E. uniflora share no coevolutionary history, having arisen on two separate continents and come into contact on a third. Our study is the first to document negative population-level effects for an invasive plant as a result of the introduction of a novel herbivore. Such inhibitory interactions are likely to become more prevalent as suites of previously noninteracting species continue to accumulate and new communities assemble worldwide.

Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation.

Some species have insufficient defenses against climate change, emerging infectious diseases, and non-native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non-native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long-term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth (Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change-induced range shifts.

Bottom-up and top-down effects on insect herbivores do not vary among sites of different salinity.

It has been suggested, but rarely tested, that the relative strength of top-down and bottom-up factors in communities varies along an environmental stress gradient. We compared the strength of bottom-up and top-down effects on the densities of insect herbivores along a range of sites of different salinities in west-central Florida. We used a 2 x 2 factorial design with plots divided into four treatments: (1) bottom-up manipulation, where fertilizer was applied to increase plant quality; (2) top-down manipulation, where sticky traps were used to reduce the effects of natural enemies (parasitoids); (3) bottom-up and top-down manipulation, where fertilizer was applied and sticky traps were used; and (4) control plots. These plots were established along a range of salinities among seven different sites containing the salt marsh plant Borrichia frutescens. In each plot, we determined the parasitism levels and abundances of the sap sucker Pissonotus quadripustulatus, the gall maker Asphondylia borrichiae, and the lepidopteran stem borer Argyresthia spp. Gall density, Pissonotus density, and stem borer density were significantly higher in lower salinity sites, suggesting a strong effect of environmental stress. There was a significant increase of galls and Pissonotus and a marginally significant increase of bored stems on fertilized plots but not on trapped plots. There was a significant interaction of site and fertilizer on gall parasitism. There were no interactions of either treatment with salinity on herbivore densities. The general lack of interaction between salinity level and other treatments on herbivore densities contrasts with our previous result where treatment effects did vary with salinity level on a large experimentally generated salinity gradient at one site. Thus, the results of the present paper suggest that, while environmental stress can modify top-down and bottom-up effects on herbivores at single sites, variation in site-to-site factors, possibly including clonal identity of plant, affects herbivore densities so much as to swamp out any observable interaction between environmental stress and top-down or bottom-up factors.

Nitrogen cycling during seven years of atmospheric CO2 enrichment in a scrub oak woodland.

Experimentally increasing atmospheric CO2 often stimulates plant growth and ecosystem carbon (C) uptake. Biogeochemical theory predicts that these initial responses will immobilize nitrogen (N) in plant biomass and soil organic matter, causing N availability to plants to decline, and reducing the long-term CO2-stimulation of C storage in N limited ecosystems. While many experiments have examined changes in N cycling in response to elevated CO2, empirical tests of this theoretical prediction are scarce. During seven years of postfire recovery in a scrub oak ecosystem, elevated CO2 initially increased plant N accumulation and plant uptake of tracer 15N, peaking after four years of CO2 enrichment. Between years four and seven, these responses to CO2 declined. Elevated CO2 also increased N and tracer 15N accumulation in the O horizon, and reduced 15N recovery in underlying mineral soil. These responses are consistent with progressive N limitation: the initial CO2 stimulation of plant growth immobilized N in plant biomass and in the O horizon, progressively reducing N availability to plants. Litterfall production (one measure of aboveground primary productivity) increased initially in response to elevated CO2, but the CO2 stimulation declined during years five through seven, concurrent with the accumulation of N in the O horizon and the apparent restriction of plant N availability. Yet, at the level of aboveground plant biomass (estimated by allometry), progressive N limitation was less apparent, initially because of increased N acquisition from soil and later because of reduced N concentration in biomass as N availability declined. Over this seven-year period, elevated CO2 caused a redistribution of N within the ecosystem, from mineral soils, to plants, to surface organic matter. In N limited ecosystems, such changes in N cycling are likely to reduce the response of plant production to elevated CO2.

Larval Dispersion and Survivorship in a Leaf-Mining Moth.

We observed and quantified leaf miner distribution on Quercus geminata in order to determine its relation to leaf abscission and the effects of leaf abscission on larvae. A leaf-mining moth, Stilbosis quadricustatella, exhibited a clumped distribution of mines among leaves of the evergreen oak Quercus geminata. Mines tended to be on large, peripheral, and undamaged leaves so that leaves were often multiply minded. Mined leaves, especially those with multiple mines, tended to abscise early. Unless miners in an abscised leaf were very near to pupation, abscission killed them. Premature leaf fall was by far the largest source of larval mortality for this moth. A preliminary analysis suggested that the clumping of miners was no more favorable to the tree (in terms of number of leaves abscised early) than to the insect.

The influence of species identity and herbivore feeding mode on top-down and bottom-up effects in a salt marsh system.

In this study we investigated the potential importance of species identity and herbivore feeding mode in determining the strengths of top-down and bottom-up effects on phytophagous insect densities. In 1998, we conducted two factorial field experiments in which we manipulated host plant quality and intensity of parasitoid attack on three salt marsh herbivores, the planthoppers Prokelisia marginata and Pissonotus quadripustulatus (Homoptera: Delphacidae), which feed only on Spartina alterniflora and Borrichia frutescens, respectively, and the gall fly Asphondylia borrichiae (Diptera: Cecidomyiidae), which feeds only on B. frutescens. We increased plant quality through addition of nitrogen fertilizer, and decreased parasitism by trapping hymenopteran parasitoids continuously throughout the study. Herbivore densities were censused biweekly. Increasing plant quality through fertilization increased the density of all three herbivores within 2 weeks of treatment application, and higher densities were maintained for the duration of the study. Reduction of top-down pressure had no effect on either planthopper species, possibly because of compensatory mortality affecting the two species. In contrast, reduction of parasitism significantly increased the density of A. borrichiae galls, perhaps because development within gall tissue reduces the sources of compensatory mortality affecting this species. The results of this study show that the bottom-up effects of plant quality were strong and consistent for all three species, but the strength of top-down effects differed between the two feeding guilds. Thus, even for herbivores feeding on the same host plant, conclusions drawn regarding the relative importance of top-down and bottom-up effects may vary depending upon the feeding mode of the herbivore.