Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory

In fragmented landscapes plant species are often confined to remnants of formerly more widespread habitats, with many of their populations being small and isolated. This study experimentally examined the effects of population size and isolation on pollination, herbivory and reproductive success in the forest herb Phyteuma spicatum (Campanulaceae). In an experiment in which population size and isolation were manipulated using plants from the same origin, population size positively affected pollinator visitation, but did not alter the generally high levels of herbivory. As a result, seed production was higher in large populations. Conversely, plants originating from 14 natural populations of varying size and degree of isolation did not differ in reproductive success when grown in the same environment, suggesting similar attractiveness to pollinators and reproductive potential. The intensity of herbivory, however, was higher in progeny of small populations, at least in terms of the proportion of biomass removed. In both experiments, there were no effects of population isolation. The results suggest (1) that small population size decreases reproductive success via direct negative effects on plant-pollinator interactions, (2) that this pattern is not offset by herbivory, but (3) that herbivory enforces fragmentation effects on pollination by further reducing the number of flowering individuals and (4) that habitat fragmentation may influence plant fitness by affecting plant response to herbivory. The effects of habitat fragmentation on plant populations in present-day landscapes are thus complex, illustrating the need for more integrated studies in conservation biology that take into account both mutualistic and antagonistic plant-animal interactions.     

Soil arthropods beneficially rather than detrimentally impact plant performance in experimental grassland systems of different diversity

Impacts of belowground insecticide application on plant performance and changes in plant community structure almost uniformly have been ascribed to reduced belowground herbivory, although recent studies reported distinct side effects on detritivore soil animals, particularly on Collembola. Consequently, it remains controversial if the resulting soil feedbacks on plants are due to alterations in arthropod herbivory or to changes in the activity of detritivores. We investigated the impacts of the application of a commonly used belowground insecticide (chlorpyrifos) on soil animals and soil feedbacks on model plant species representing two main plant functional groups of grassland communities, the grass Lolium perenne and the forb Centaurea jacea.Insecticide application decreased soil insect herbivore densities considerably. However, also Collembola densities and diversity decreased markedly due to insecticide application and this was most pronounced in Entomobryidae, Isotomidae, Hypogastruridae, and Sminthuridae. While densities of other detritivore taxa were not affected or even increased (Oribatida) in insecticide subplots, that of predators mostly decreased.Both model plant species built considerably more biomass in control subplots than in insecticide subplots irrespective of characteristics of the resident plant community. This suggests that soil feedbacks on plants were not due to belowground herbivory and highlights the significance of alternative mechanisms responsible for insecticide-mediated soil feedbacks on plants. The deterioration of model plant species’ performances in insecticide subplots most likely was due to decreased densities of Collembola resulting in the deceleration of nutrient cycling and plant nutrition. The results suggest that it is oversimplistic to only ascribe insecticide-mediated soil feedbacks on plants to belowground herbivores. The results further indicate that in the present study the impact of arthropod detritivores on plant productivity was more important than that of belowground herbivores. This emphasizes that plant-soil arthropod interactions in grassland might be based on both facilitative and antagonistic interrelationships.     

Integrating demographic and genetic approaches in plant conservation

We summarize the problems that populations of formerly common plants may encounter when habitat fragmentation isolates them and reduces population size. Genetic erosion, inbreeding depression, Allee-effects on reproductive success, catastrophes and environmental stochasticity are illustrated with studies on species that have recently become rare in The Netherlands due to habitat fragmentation. These clearly indicate that population viability is negatively affected. We also show that in the recent literature (since 1980), most studies on the conservation of rare plants have addressed population genetic structure and relationships between genetic variation and population size. Though important, these studies are not suitable for assessing the importance of genetics for population viability. In turn, demographic studies can detect changes in vital rates in small populations, but cannot reveal underlying genetic causes. Fitness and demographic studies are also well-represented in the literature, but remarkably few studies have attempted to integrate empirical demographic and genetic studies. We discuss two approaches to fill this very important lacuna in our knowledge. One of these constructs matrix-projection models on the basis of demographic censuses of—if possible—large and viable populations, and combines these with the results of experiments to determine inbreeding effects on demographic transitions and, subsequently, population growth and extinction. The other approach is to demographically monitor experimentally created small and large populations with low and high genetic variation and measure their actual growth rates and probabilities of extinction. We conclude that demography and demographic-genetic experiments should play a central role in plant conservation genetics.     

Identifying rarity in insects: the importance of host plant range

Some phytophagous insects are rare because their host plants are rare. This study uses data on the distribution of plants and insects from Great Britain to establish whether a threshold exists for the geographical range of a host plant below which its specific insects can be consistently described as rare. Data on four well-studied insect taxa (macro-moths, gelechiid micro-moths, beetles, and tephritid flies) that have been afforded conservation status as Red Data Book (RDB) or scarce (nationally Notable-A and -B) are examined. The proportion of species that are rare in these taxa declines as host plant range increases. Extrapolating these patterns of host range/phytophagous insect rarity to less studied groups (aphids, agromyzid flies and tortricid micro-moths) identifies a large number of insects that are probable candidates for conservation. Empirical evidence supports the view that many of the species selected by this process are indeed rare and in need of conservation. Identifying a host plant range below which insect herbivores are therefore rare provides an economical and objective method for producing a shortlist of phytophagous insect species rare enough to warrant conservation measures.     

Determinants of reproductive success: A comparative study of five endangered river corridor plants in fragmented habitats

River corridor plants in Central Europe have in recent decades become increasingly rare, caused mainly by habitat destruction and change. The aim of this study was to examine the impact of soil quality, but especially of habitat fragmentation in terms of population size and isolation, on seed production and germination of five selected species, all of which being endangered, perennial herbs: Euphorbia palustris, Lathyrus palustris, Pseudolysimachion longifolium, Sanguisorba officinalis, and Senecio paludosus. We sampled totally 58 populations in flood plains in the surroundings of Bremen, North-western Germany.

In all five species, there were positive correlations between the number of seeds (total seed mass) and plant height, as well as between germination and seed mass. Seed traits values and/or germination were negatively affected by small population size, in Euphorbia, Lathyrus and Pseudolysimachion additionally by high population isolation. There were also significant effects of soil quality, but these were less consistent across species. The contribution of population size and isolation, compared to soil quality, to the variance explained in the reproductive components was especially high in Euphorbia and Lathyrus, the only two species depending on insect pollination.

The results indicate that the five species are likely to decline as a consequence of decreased plant fitness in small and/or isolated populations, probably caused by pollen limitation. The studied species may be representative for the group of river corridor plants as a whole that are often restricted to isolated remnants of near-natural flood plain vegetation in a matrix of heavily used agricultural land.     

Effects of community-level grassland management on the non-target rare annual Agalinis auriculata

The objective of grassland management is to maintain keystone species, as well as species diversity, to promote a particular community structure, or to preserve specific ecosystem processes. Studies of grassland management rarely ascertain the effects on rare plant species, although conservation plans for rare herbaceous plants often recommend habitat management as well as restoration activities. Indeed, conservation biology has evolved from a relatively species-specific discipline into one more focused on larger scale issues such as ecosystem function, community composition and habitat restoration. Few studies have tested whether species of concern are adequately managed with a community or ecosystem-level approach. In this study, we evaluate whether community-level management of white-tailed deer and woody brush improves the viability of the rare annual plant species, Agalinis auriculata (Earleaf false foxglove; Orobanchaceae). Reducing deer browse and removing brush each positively affect plant vital rates. Brush removal increases the proportion of plants that reach the largest size class. Reducing deer browse increases the fertility of plants, particularly those in the largest size class. We report on demographic matrix models created with data from five populations of A. auriculata studied across 4 years. We find that both management activities positively affect the non-target plant species and are, in fact, necessary for A. auriculata to persist. Conservation of A. auriculata at our study sites requires both reducing the density of white-tailed deer and brush removal. Our study demonstrates that management at the community and ecosystem levels can be compatible with conservation goals at the species and population levels.     

Long-term response of spring flora to chronic herbivory and deer exclusion in Great Smoky Mountains National Park, USA

Chronic herbivory by white-tailed deer (Odocoileus virginianus Zimmerman) can have profound impacts on the function and structure of forest ecosystems. We examined the combined influence of intense herbivory associated with a deer population eruption and chronic herbivory by the post eruption population on the spring flora of Cades Cove, Great Smoky Mountains National Park. During the 1970s the deer population reached a peak of 43 deer per km², from which it has slowly declined in recent decades. To examine the influence of intense herbivory, we compared the abundance and flowering rates of early flowering plants in Cades Cove to a nearby reference site with similar bedrock geology, vegetation, and disturbance history but contrasting history of deer abundance. Our results suggest that significant changes (p ? 0.05) in the diversity, evenness, and species richness of the spring flora occurred during the eruptive phase. Trillium spp. and other liliaceous species appeared to be disproportionately impacted. Comparisons between control and exclosure plots established after the deer population eruption indicate that recovery has been largely restricted to species that were able to persist under intense herbivory. These species have increased in number in exclosures, suggesting continued impacts by deer on the plant community outside the exclosures. Little to no recolonization by browse sensitive species was observed. Consequently, to restore the natural diversity of early flowering plants once present in Cades Cove, active restoration may be necessary in addition to maintaining deer densities below current levels.     

Meta-analysis on the association of population size and life history with inbreeding depression in plants

Inbreeding is common in plants and can have considerable effects on population viability, because of inbreeding depression. Understanding what determines the magnitude of inbreeding depression is of fundamental importance for conservation biology. We used meta-analysis of 116 studies and 107 plant species to investigate the effects of population size, test environment, life history characteristics and stage on the magnitude of inbreeding depression in 13 different fitness traits. We found that inbreeding depression levels significantly increase with population size. This may be a consequence of either, or both, a higher baseline of the level of inbreeding or increased impact of purging in small populations; unfortunately the available data did not allow distinguishing between these potential explanations. In general, inbreeding depression was found to be common across species and environments, and was significant in all traits examined. Yet, the magnitude of inbreeding depression was significantly influenced by plant longevity and life-history stage, and varied depending on how plant fitness was measured. Our findings highlight the fundamental role of population size in influencing the magnitude of inbreeding depression in plants. This clearly has important implications for conservation biology. Moreover, our findings on the overall generality of inbreeding depression confirm that inbreeding depression is one of the key factors reducing plant population fitness and viability. Hence, we need a better understanding on the architecture of inbreeding depression, how different ecological and historical conditions influence the levels of inbreeding depression in natural plant populations, and its impacts on community dynamics.     

Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems

Cultural methods such as crop fertilization can affect susceptibility of plants to insect pests by altering plant tissue nutrient levels. Research shows that the ability of a crop plant to resist or tolerate insect pests and diseases is tied to optimal physical, chemical and mainly biological properties of soils. Soils with high organic matter and active soil biology generally exhibit good soil fertility. Crops grown in such soils generally exhibit lower abundance of several insect herbivores, reductions that may be attributed to a lower nitrogen content in organically farmed crops. On the other hand, farming practices, such as excessive use of inorganic fertilizers, can cause nutrient imbalances and lower pest resistance. More studies comparing pest populations on plants treated with synthetic versus organic fertilizers are needed. Understanding the underlying effects of why organic fertilization appears to improve plant health may lead us to new and better integrated pest management and integrated soil fertility management designs.     

Effects of Key deer herbivory on forest communities in the lower Florida Keys

Ungulate herbivory can have strong impacts on plant communities, but these impacts are rarely considered in recovery plans of endangered species. This study examined the effects of the endangered Key deer (Odocoileus virginianus clavium) on its environment in the lower Florida Keys. The Key deer population has increased to over 700 deer from approximately 50 deer in the 1950s; however, approximately 75% of the population resides on only a few islands (Big Pine, No Name, Big Munson) where Key deer herbivory on forest communities may be substantial. Effects of deer herbivory on plant densities were estimated on these islands using vegetation quadrats in hardwood hammock, buttonwood transition, and mangrove wetlands and compared to nine other islands with intermediate or low deer densities. On islands with high deer density, densities of preferred woody plant species <1.2 m tall (within Key deer reach) were significantly lower than islands with lower deer densities, while densities of some nonpreferred species were significantly higher. Deer exclosures established in hardwood hammock on a high-density deer island revealed a mean increase in abundance/height of preferred woody species inside exclosures, while nonpreferred species significantly increased in open plots. We conclude that on high deer density islands, highly preferred plant species might eventually fail to regenerate and unpalatable plant species may become dominant. Careful criteria need to be developed to maintain Key deer numbers above an endangered species status yet below levels that are destructive to local forest species.     

Is the collection of Aloe peglerae from the wild sustainable? An evaluation using stochastic population modelling

Aloe peglerae Schönland, an Endangered species endemic to South Africa, is threatened mainly by illegal collection. Lower densities of plants in areas easily accessible to the public led to questions concerning the sensitivity of this species to collection. Demographic monitoring data collected between 1976 and 1995 were used to build a stochastic population model, where parameters were allowed to vary randomly between observed minimum and maximum values. The model indicated that A. peglerae is highly sensitive to harvest of adult plants, with use sustainable at only very low levels of not more than 0.12%. Harvesting one plant annually is only sustainable in large populations of more than 1000 individuals; populations of this size, however, are rare. A maximum of fifteen percent of the annual seed output can be harvested sustainably. This long-term evaluation demonstrates that current collection of this species from the wild is unsustainable. Ex situ cultivation is therefore vital.     

Herbivore and pollinator responses to grassland management intensity along experimental changes in plant species richness

Agricultural intensification is a major driver of global environmental change. Disentangling the relative impact of losses in plant species richness and intensified management on higher trophic level organisms is important for conservation recommendations.We established different management regimes along an experimental gradient of plant species richness within “The Jena-Experiment” in Germany and quantified herbivory as well as grasshoppers and pollinators. Herbivory, grasshopper density and species richness and frequency of flower visiting pollinators were recorded two times in each of four subplots of altogether 80 plots differing in plant species richness. Each of the four subplots was subject to four different levels of fertilizer application and mowing to simulate very low, low, high and very high land use intensity.Fertilization and mowing significantly affected plant–herbivore interactions but plant species richness had no discernible effect. Grasshoppers were most abundant at high intensity subplots (3.1 individuals per m²) and least abundant on very low intensity subplots (1.3 individuals per m²). Leaf damage caused by herbivores was highest in even the very high intensity subplots (3.7%) with four mowing events per year and high amounts of fertilizer application and lowest on subplots with a low management intensity (2.4%) comprising two mowing events per year but no fertilizer application. In contrast, pollinators benefited most from lower management intensities, with only one or two mowing events and no fertilizer addition. In addition, higher numbers of flowering plant species and increased blossom cover was associated with enhanced pollinator species richness and flower visitation.Our results indicate that even in grasslands with high plant species richness, mowing and fertilization are more important drivers of herbivory and flower visitation by pollinators. Management with no more than two cuts per year and without fertilizer application in our grasslands balanced the ecosystem functions of increased pollination and decreased herbivory.     

Insect communities and biotic interactions on fragmented calcareous grasslands—a mini review

We evaluate existing evidence for alternative hypotheses on the effects of fragmentation with special emphasis on insects of calcareous grasslands. Species richness of butterflies in general and the proportion of monophagous species in particular increase with fragment size. Habitat fragmentation disrupts plant-pollinator and predator—prey interactions in some cases. No evidence for changes in the outcome of competitive interactions exists for insects. Habitat connectivity increases inter-patch movement and population density and decreases extinction risk. Habitat quality changes with succession and management. Depending on life-history traits, insect species may profit from early, mid or late successional stages of calcareous grasslands. We conclude from the few well-designed and replicated studies that there is a bias towards modelling approaches and small-scale fragmentation experiments, so more large-scale studies on a community level are needed to quantify the functional roles of insects and their dependence on fragmented calcareous grasslands in the landscape mosaic.     

An evaluation of the status of five threatened plant species in the Pyrenees

In this paper we assess the conservation status of five of the most threatened species in the Pyrenean range (listed in the European Habitats Directive), and present updates of their distribution, reliable censuses to estimate population sizes, population growth rate, population structure, longevity, reproductive success and frequency of herbivory. Recent surveys and careful censuses revealed that the four taxa exclusively restricted to rocky habitats (Borderea chouardii, Androsace pyrenaica, Petrocoptis pseudoviscosa, Petrocoptis montsicciana) have more populations and/or individuals than previously thought. The remaining species, an orchid (Cypripedium calceolus), showed an important decline in population number. So while the rupicolous taxa might be considered naturally rare, the orchid is becoming rare. We failed to find evidence of current poor performance within populations, as recruitment was detected, population growth rate was quite stable in recent years, fruit and seed set was apparently adequate, and herbivory and predation were absent or very low. Additionally, most of the species show a long life span, which might buffer them against demographic and environmental stochasticity in absence of human disturbance.     

Genetic and demographic responses of fragmented Acacia dealbata (Mimosaceae) populations in southeastern Australia

Genetic and demographic studies of fragmented populations of common plant species often reveal negative impacts that are likely to constrain persistence. Examining species that are broadly representative of functional groups within fragmented landscapes is one approach to providing a better understanding of how these processes will influence vegetation persistence. Acacias are a significant component of the Australian flora, with Acacia dealbata being a common and representative species of fragmented landscapes across New South Wales. Previous reproductive assessments of fragmented A. dealbata populations indicated significant constraints for small populations through low reproductive output mediated by fertilisation success. This study examined genetic diversity, mating system, and progeny growth parameters of the seed crops produced by these populations to assess whether further constraints to persistence could be detected. Spatially explicit simulation studies were also conducted to assess the persistence likelihood of fragmented populations. Landscape parameters such as population size and plant density were useful predictors for some of the genetic and demographic responses, but a poor response signal was generally observed. Strong evidence for a self-incompatibility mechanism was observed in A. dealbata and is likely to be the major driver of population persistence. Self-incompatibility in small populations limits mate availability and eliminates inbred progeny early in the reproductive cycle leading to poor reproductive output. The simulation data provides further evidence that mate limitation in smaller populations (<200 plants and 40 S alleles) constrains reproductive output and persistence. These data indicate that introducing new germplasm to smaller populations can dramatically improve their persistence likelihood.     

Phytochemical induction by herbivores could affect quality of essential oils from aromatic plants

Plant tissues may show chemical changes following herbivory. In aromatic plants such changes could affect the specific compounds on which commercial exploitation is based. This possibility was analyzed for Mintosthachys mollis, a member of the Lamiaceae native to Central Argentina with medicinal and aromatic uses in the region, and two types of insect herbivores: a leaf miner and a gall insect. Analysis of the essential oils of mined/undamaged leaves, as well as leaves from stems with and without galls, revealed changes in concentrations of the two main monoterpenes. A decrease in pulegone concentration was associated with both types of insect damage, whereas menthone increased significantly only in mined leaves. Inducible chemical changes in aromatic and medicinal plants may be common and widespread; their economic implications deserve investigation.     

The regeneration status of the endangered Acer opalus subsp. granatense throughout its geographical distribution in the Iberian Peninsula

Acer opalus subsp. granatense is an endemic endangered tree with a wide but fragmented distribution in the Mediterranean mountains. The persistence of its small populations often depends on just a few adults, and consequently is highly vulnerable to factors limiting recruitment. In this paper, we examined the regeneration status of this maple in 16 populations throughout its whole geographical distribution in the Iberian Peninsula. Age and size structures were analysed as indicators of the viability of the species. Additionally, we studied the effects of herbivory by ungulates and the role of shrubs as nurse plants in maple regeneration dynamic. Our results show that A. opalus subsp. granatense has active recruitment throughout its range in the Iberian Peninsula. Shrubs served as the main microsites for recruitment, not only for early establishment but also for long-term survival. However, ungulates heavily damaged maple saplings in all locations and microhabitats. A direct consequence of herbivory is the uncoupling of age and size structures, saplings becoming older but not higher, possibly affecting population turnover in the long term. We suggest that the conservation of the small populations of Acer opalus subsp. granatense heavily depends on the control of herbivory pressure throughout the maple distribution area.     

Resolving conflicts between butterfly host resource abundance and genet population size estimates for a vegetatively spreading, threatened grassland legume

Population size estimates are an integral part of rare plant conservation, but common abundance measurements such as cover and ramet number may not accurately index genet population size for vegetatively spreading species. Population monitoring of Kincaid’s lupine (threatened species) populations occurs through genet-anonymous leaf cover and raceme counts despite extensive, non-adventitious rhizome growth. While the current monitoring scheme provides important resource abundance measurements for the endangered Fender’s blue butterfly, whose larvae feed on Kincaid’s lupine leaves, the methods are not appropriate for estimating lupine genet number. Major axis regression revealed well supported statistical relationships between cover, raceme, and plantlet (a measurement of modular plant growth) density within six study patches (n = 3 populations) of Kincaid’s lupine (R² > 0.90) and when all patch data were combined (R² > 0.91). Genet population size estimates from genotype only data with ACE (an estimator used to infer species richness) were similar to estimates derived from a combination of plantlet density and genet to plantlet ratios (genotype derived) in small, more thoroughly genotyped lupine patches. However, genet number estimates from ACE were 3–5-fold greater in less intensely genotyped patches. Genet-anonymous plant abundance measurements, such as cover, can be used to estimate genet number in populations of vegetatively spreading plants provided they are calibrated with a unit of modular plant growth. Calibration of vegetative measurements, consistency of between population relationships, and closer scrutiny of highly supported statistical models may be necessary to develop more pertinent monitoring methods for rare, vegetatively spreading plants.     

Slow-cycle effects of foliar herbivory alter the nitrogen acquisition and population size of Collembola

In terrestrial systems there is a close relationship between litter quality and the activity and abundance of decomposers. Therefore, the potential exists for aboveground, herbivore-induced changes in foliar chemistry to affect soil decomposer fauna. These herbivore-induced changes in chemistry may persist across growing seasons. While the impacts of such slow-cycle, ‘legacy’ effects of foliar herbivory have some support aboveground, such impacts have not been evaluated for soil invertebrates. Here, we investigate legacy effects on Collembola population structure and nitrogen acquisition. We collected foliar material (greenfall) from trees that had, in the preceding season, been exposed to insect herbivory by leaf-chewing Lepidoptera. Collembola populations were grown with the greenfall in soil microcosms across 16 weeks. While there were only modest effects of herbivory on the greenfall mass loss, Collembola abundance and biomass after 8 weeks of greenfall exposure were approximately 2.5-fold greater in the controls. Given that Collembola biomass percentage nitrogen was relatively fixed, this translated to approximately 2.5-fold greater biomass nitrogen. The herbivore treatment decreased the absolute amount of Collembola biomass nitrogen derived from both greenfall and soil, and the relative contribution of litter nitrogen and soil nitrogen to Collembola biomass nitrogen was dependent on both the herbivory treatment and greenfall initial nitrogen. Our results show that slow-cycle, legacy effects of foliar herbivory may affect soil faunal population structure and nitrogen acquisition, demonstrating the potential for aboveground herbivory to influence belowground animal ecology and nitrogen cycling across multi-annual timescales.