Differential responses of vertebrate and invertebrate herbivores to traits of New Zealand subalpine shrubs

Plant traits are influenced by herbivore diet selection, but little is known about how traits are affected by different types of herbivores. We related eight traits of 27 subalpine shrub species in South Island, New Zealand, to damage of these shrubs by introduced red deer (Cervus elaphus) and native invertebrate herbivores using phylogenetically explicit modeling. Deer preferentially consumed species that grew quickly, were low in foliar tannins, or had high leaf area per unit mass. However, these traits did not trade off against each other; rather, they could be related to different multivariate defense strategies. Although the proportion of leaves damaged by leaf-chewing invertebrates also increased with stem growth, invertebrates did not damage the same fast growing species as those preferred by deer. Other traits may also be important in determining herbivore preferences, as suggested by the high proportion of variation in herbivory explained by phylogeny. Last, we found that the composition of invertebrate herbivore communities was more similar among closely related shrubs, and consequently, the range of invertebrate-plant associations may change if introduced deer shift plant composition toward slow-growing species. Overall, our results demonstrate the importance of herbivore type and coevolved interactions for the adaptive significance of plant traits.     

Indirect Effects of Pandemic Deer Overabundance Inferred from Caterpillar‐Host Relations

Externally feeding phytophagous insect larvae (i.e., caterpillars, here, larval Lepidoptera and sawflies, Hymenoptera: Symphyta) are important canopy herbivores and prey resources in temperate deciduous forests. However, composition of forest trees has changed dramatically in the eastern United States since 1900. In particular, browsing by high densities of white‐tailed deer (Odocoileus virginianus) has resulted in forests dominated by browse‐tolerant species, such as black cherry (Prunus serotina), and greatly reduced relative abundance of other tree species, notably pin cherry (Prunus pensylvanica) and birches (Betula spp.). To quantify effects of these changes on caterpillars, we sampled caterpillars from 960 branch tips of the 8 tree species that comprise 95% of trees in Allegheny hardwood forests: red maple (Acer rubrum), striped maple (Acer pensylvanicum), sugar maple (Acer saccharum), sweet birch (Betula lenta), yellow birch (Betula allegheniensis), American beech (Fagus grandifolia), black cherry, and pin cherry. We collected 547 caterpillar specimens that belonged to 66 Lepidoptera and 10 Hymenoptera species. Caterpillar density, species richness, and community composition differed significantly among tree species sampled. Pin cherry, nearly eliminated at high deer density, had the highest density and diversity of caterpillars. Pin cherry shared a common caterpillar community with black cherry, which was distinct from those of other tree hosts. As high deer density continues to replace diverse forests of cherries, maples, birches, and beech with monodominant stands of black cherry, up to 66% of caterpillar species may be eliminated. Hence, deer‐induced changes in forest vegetation are likely to ricochet back up forest food webs and therefore negatively affect species that depend on caterpillars and moths for food and pollination. Efectos Indirectos de la Sobreabundancia de Venados Pandémicos Inferida de Relaciones Orugas‐Huéspedes     

Experimental test of parasitism hypothesis for population cycles of a forest lepidopteran

Population cycles of herbivores are thought to be driven by trophic interaction mechanisms, either between food plant and herbivore or between the herbivorous prey and its natural enemies. Observational data have indicated that hymenopteran parasitoids cause delayed density-dependent mortality in cyclic autumnal moth (Epirrita autumnata) populations. We experimentally tested the parasitism hypothesis of moth population cycles by establishing a four-year parasitoid-exclusion experiment, with parasitoid-proof exclosures, parasitoid-permeable exclosures, and control plots. The exclusion of parasitoids led to high autumnal moth abundances, while the declining abundance in both the parasitoid-permeable exclosures and the control plots paralleled the naturally declining density in the study area and could be explained by high rates of parasitism. Our results provide firm experimental support for the hypothesis that hymenopteran parasitoids have a causal relationship with the delayed density-dependent component required in the generation of autumnal moth population cycles.     

Invasional meltdown: invader-invader mutualism facilitates a secondary invasion

In multiply invaded ecosystems, introduced species should interact with each other as well as with native species. Invader-invader interactions may affect the success of further invaders by altering attributes of recipient communities and propagule pressure. The invasional meltdown hypothesis (IMH) posits that positive interactions among invaders initiate positive population-level feedback that intensifies impacts and promotes secondary invasions. IMH remains controversial: few studies show feedback between invaders that amplifies their effects, and none yet demonstrate facilitation of entry and spread of secondary invaders. Our results show that supercolonies of an alien ant, promoted by mutualism with introduced honeydew-secreting scale insects, permitted invasion by an exotic land snail on Christmas Island, Indian Ocean. Modeling of land snail spread over 750 sites across 135 km2 over seven years showed that the probability of land snail invasion was facilitated 253-fold in ant supercolonies but impeded in intact forest where predaceous native land crabs remained abundant. Land snail occurrence at neighboring sites, a measure of propagule pressure, also promoted land snail spread. Site comparisons and experiments revealed that ant supercolonies, by killing land crabs but not land snails, disrupted biotic resistance and provided enemy-free space. Predation pressure on land snails was lower (28.6%), survival 115 times longer, and abundance 20-fold greater in supercolonies than in intact forest. Whole-ecosystem suppression of supercolonies reversed the probability of land snail invasion by allowing recolonization of land crabs; land snails were much less likely (0.79%) to invade sites where supercolonies were suppressed than where they remained intact. Our results provide strong empirical evidence for IMH by demonstrating that mutualism between invaders reconfigures key interactions in the recipient community. This facilitates entry of secondary invaders and elevates propagule pressure, propagating their spread at the whole-ecosystem level. We show that identification and management of key facilitative interactions in invaded ecosystems can be used to reverse impacts and restore resistance to further invasions.     

A Natural Experiment on the Impact of Overabundant Deer on Forest Invertebrates

Abstract:  In large parts of North America and Europe, deer overabundance threatens forest plant diversity. Few researchers have examined its effects on invertebrate assemblages. In a natural experiment on Haida Gwaii (British Columbia, Canada), where Sitka black-tailed deer ( Odocoileus hemionus sitkensis ) were introduced, we compared islands with no deer, with deer for fewer than 20 years, and with deer for more than 50 years. We sampled invertebrates in three habitat categories: forest edge vegetation below the browse line, forest interior vegetation below the browse line, and forest interior litter. In forest edge vegetation, invertebrate abundance and species density decreased with increasing length of browsing history. In forest interior vegetation, decrease was significant only on islands with more than 50 years of browsing. Insect abundance in the vegetation decreased eightfold and species density sixfold on islands browsed for more than 50 years compared with islands without deer. Primary consumers were most affected. Invertebrates from the litter showed little or no variation related to browsing history. We attributed the difference between vegetation-dwelling and litter-dwelling invertebrates to differences in the effect of browsing on their habitat. In the layer below the browse line deer progressively removed the habitat. The extent of litter habitat was not affected, but its quality changed. We recommend more attention be given to the effect of overabundant ungulates on forest invertebrate conservation with a focus on edge and understory vegetation in addition to litter habitat.     

Effects of Karst Forest Degradation on Pulmonate and Prosobranch Land Snail Communities in Sabah, Malaysian Borneo

Abstract:  Limestone (karst) outcrops in Southeast Asia are rich in land snails. Certain groups of land snails, in particular Prosobranchia species, are restricted to limestone and show a high degree of short-range endemism. Karst habitats are, however, seriously degraded by quarrying, logging, agriculture, and burning. The effect of these disturbances on land snail fauna is unknown, so we studied paired primary and secondary forest localities on six separate limestone hills in Sabah, Malaysian Borneo. Land snails were sampled with a standard protocol and identified to species level. More than 16,000 individuals, belonging to 74 species, were recorded. In most sites, snail diversities did not differ between disturbed and undisturbed plots. However, pulmonate snails were significantly more abundant at disturbed localities than prosobranch snails, whereas abundances for both groups were similar at undisturbed sites. Because Prosobranchia contain many site-endemic species, our findings suggest that continued exposure to these disturbances will eventually lead to extinctions in this group.     

Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni

Generalized, facultative mutualisms are often characterized by great variation in the benefits provided by different partner species. This variation may be due to differences among species in the quality and quantity of their interactions, as well as their phenology. Many plant species produce extrafloral nectar, a carbohydrate-rich resource, to attract ant species that can act as "bodyguards" against a plant's natural enemies. Here, we explore differences in the quality and quantity of protective service that ants can provide a plant by contrasting the four most common ant visitors to Ferocactus wislizeni, an extrafloral nectary-bearing cactus in southern Arizona. The four species differ in abundance when tending plants, and in the frequency at which they visit plants. By adding surrogate herbivores (Manduca sexta caterpillars) to plants, we demonstrate that all four species recruit to and attack potential herbivores. However, their per capita effectiveness in deterring herbivores (measured as the inverse of the number of workers needed to remove half of the experimentally added caterpillars) differs. Using these among-species differences in quality (per capita effectiveness) and quantity (number of workers that visit a plant and frequency of visitation), we accurately predicted the variation in fruit production among plants with different histories of ant tending. We found that plant benefits (herbivore removal and maturation of buds and fruits) typically saturated at high levels of ant protection, although plants could be "well defended" via different combinations of interaction frequency, numbers of ant workers per interaction, and per capita effects. Our study documents variation among prospective mutualists, distinguishes the components of this variation, and integrates these components into a predictive measure of protection benefit to the plant. The method we used to average saturating benefits over time could prove useful for quantifying overall service in other mutualisms.     

Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations

Species may compete indirectly by altering the traits of a shared resource. For example, herbivore-induced responses in plants may make plants more resistant or susceptible to additional herbivorous insect species. Herbivore-induced plant responses can significantly affect interspecific competition and herbivore population dynamics. These herbivore-herbivore indirect interactions have been overlooked in aquatic ecosystems where previous studies used the same herbivore species to induce changes and to assess the effects of these changes. We asked whether seaweed grazing by one of two herbivorous, congeneric snail species (Littorina obtusata or Littorina littorea) with different feeding strategies and preferences would affect subsequent feeding preferences of three herbivore species (both snails and the isopod Idotea baltica) and population densities of three herbivore species (both snails and a third periwinkle snail, Lacuna vincta). In addition, we measured phlorotannin concentrations to test the hypothesis that these metabolites function as induced defenses in the Phaeophyceae. Snail herbivory induced cue-specific responses in apical tissues of the seaweed Fucus vesiculosus that affected the three herbivore species similarly. When compared to ungrazed controls, direct grazing by Littorina obtusata reduced seaweed palatability by at least 52% for both snail species and the isopod species. In contrast, direct grazing by L. littorea did not decrease seaweed palatability for any herbivore, indicating herbivore-specific responses. Previous grazing by L. obtusata reduced populations of L. littorea on outplanted seaweeds by 46% but had no effect on L. obtusata populations. Phlorotannins, a potential class of inducible chemicals in brown algae, were not more concentrated in grazed seaweed tissues, suggesting that some other trait was responsible for the induced resistance. Our results indicate that marine herbivores may compete via inducible responses in shared seaweeds. These plant-mediated interactions were asymmetric with a specialist (L. obtusata) competitively superior to a generalist (L. littorea).     

Plant invasions, generalist herbivores, and novel defense weapons

One commonly accepted mechanism for biological invasions is that species, after introduction to a new region, leave behind their natural enemies and therefore increase in distribution and abundance. However, which enemies are escaped remains unclear. Escape from specialist invertebrate herbivores has been examined in detail, but despite the profound effects of generalist herbivores in natural communities their potential to control invasive species is poorly understood. We carried out parallel laboratory feeding bioassays with generalist invertebrate herbivores from the native (Europe) and from the introduced (North America) range using native and nonnative tetraploid populations of the invasive spotted knapweed, Centaurea stoebe. We found that the growth of North American generalist herbivores was far lower when feeding on C. stoebe than the growth of European generalists. In contrast, North American and European generalists grew equally well on European and North American tetraploid C. stoebe plants, lending no support for an evolutionary change in resistance of North American tetraploid C. stoebe populations against generalist herbivores. These results suggest that biogeographical differences in the response of generalist herbivores to novel plant species have the potential to affect plant invasions.     

Using Parasitic Trematode Larvae to Quantify an Elusive Vertebrate Host

Abstract: Digenean trematode parasites require multiple host species to complete their life cycles, and their abundance can often be strongly correlated with the abundance of their host species. Species richness and abundance of parasites in easily sampled host species may yield an accurate estimate of the species richness and abundance of other hosts in a parasite's life cycle that are difficult to survey directly. Accordingly, we investigated whether prevalence and mean abundance of trematodes could be used to estimate the abundance of one of their host species, diamondback terrapins (Malaclemys terrapin), which are difficult to sample and are designated as near threatened (by the International Union for Conservation of Nature [IUCN Red List]) along some U.S. coasts. As an adult the trematode Pleurogonius malaclemys is specific to terrapins. Its larval stages live first inside mud snails (Ilyanassa obsoleta) and are subsequently shed into the environment where they form external metacercarial cysts on hard surfaces such as snail opercula. The life cycle of P. malaclemys is completed when terrapins ingest these cysts. At 12 sites along the coast of Georgia (U.S.A.), we determined the prevalence of internal P. malaclemys larvae in mud snails (proportion of infected snails in a population) and the prevalence and mean abundance of external trematode cysts. We examined whether these data were correlated with terrapin abundance, which we estimated with mark‐recapture methods. The abundance of external cysts and salinity explained ≥59% of the variability in terrapin abundance. We suggest that dependent linkages between the life stages of multihost parasites make them reliable predictors of host species’ abundance, including hosts with abundances that are challenging to quantify directly.     

The disruption of an ant-aphid mutualism increases the effects of birds on pine herbivores

Predators affect herbivores directly and indirectly, by consumptive and nonconsumptive effects, and the combined influence of multiple predators is shaped by interactions among predators. I documented the individual and combined effects of birds (chickadees, nuthatches, warblers) and ants (Formica podzolica) on arthropods residing in pine (Pinus ponderosa) canopies in a factorial field experiment. Birds and ants removed herbivores but simultaneously benefited them by removing predatory arthropods. Birds and ants had net negative and positive effects, respectively, on the abundance of herbivore prey, supporting the notion that vertebrate predators have stronger negative effects on herbivores than do arthropod predators. Aphids (ant-tended and untended species) constituted three-quarters of herbivore biomass. The effect of birds on ant-tended aphids was twice that on untended aphid species or tended aphid species without ants. This was not due to there being more ant-tended aphids for birds to prey on; tended and untended aphid species were in similar abundances in the absence of birds. Instead, the effects of birds were strengthened by attributes of the mutualism that rendered tended aphids susceptible to predation. These dynamics led to nonadditive effects of birds and ants: birds only reduced tended aphid species and total herbivore abundances on trees with ants, while ants only increased tended aphid species and total herbivore abundances in the absence of birds. Consequently, top predators in this system only influenced total herbivore abundance when they disrupted an ant-aphid mutualism.     

Invasive prey impacts the abundance and distribution of native predators

While an extensive literature exists on the negative effects of invasive species, little is known about their facilitative effects on native species, particularly the role of invasives as trophic subsidies to native predators. The invasive gypsy moth (Lymantria dispar) undergoes periodic outbreaks during which it represents a super-abundant food source for predators capable of consuming it, particularly native cuckoos (Coccyzus erythropthalmus and C. americanus). We examined how gypsy moth outbreaks affect the abundance and distribution of cuckoos using the North American Breeding Bird Survey and 29 years of U.S. Forest Service gypsy moth defoliation records. Abundances of both Black-billed and Yellow-billed Cuckoos were significantly above average during outbreaks, but populations were average or below average in preceding and subsequent years, suggesting that cuckoos are immigrating to defoliations during outbreak years. Spatial analyses showed that cuckoo abundances approximately 40-150 km outside of defoliation areas were significantly below average, and these under-occupied breeding areas extended in all four compass directions around outbreaks. This result supports the idea that cuckoos locate gypsy moth outbreaks during a post-migratory nomadic phase. By shifting the annual distribution of cuckoos, gypsy moths may be shifting the trophic impact of cuckoos across large distances, which could affect native insect herbivores and plants.     

Terrestrial liming benefits birds in an acidified forest in the northeast

Studies in Europe have reported negative effects of acid deposition on forest birds, and research in North America has identified links between forest bird abundance and rates of acid deposition. We examined the bird community in an acidified forest in central Pennsylvania (USA) and evaluated the effects of terrestrial lime application on birds. We used a before-after control-impact (BACI) study design, with one year of observation before (2003) and three years after lime application (2004, 2005, and 2006). Between the 2003 and 2004 field seasons, 4500 kg/ha of dolomitic lime were applied to two of four 100-ha watersheds. Each year, we monitored bird abundance and Ovenbird (Seiurus aurocapilla) eggshell thickness and territory size. Soil and snail abundance data were also collected. The bird community and territory size results indicated that the study area may be providing low-quality habitat for forest birds, perhaps as a result of acid deposition. We found lower forest bird abundances than have been found in less acidified areas of Pennsylvania, and larger Ovenbird territory sizes than have been found in other studies. We found a significant positive relationship between soil calcium and bird abundance, indicating that soil calcium may affect bird abundance. Liming increased soil calcium and pH and led to increased snail and bird abundances. After liming, bird abundance was positively related to snail abundance. No significant changes occurred in Ovenbird territory size or eggshell thickness. Our results suggest that acid deposition could be responsible for reduced bird abundance, and that liming is a potential mitigation technique.     

Indirect effects of large herbivores on snakes in an African savanna

Many large mammal species are declining in African savannas, yet we understand relatively little about how these declines influence other species. Previous studies have shown that the removal of large herbivorous mammals from large-scale, replicated experimental plots results in a dramatic increase in the density of small mammals, an increase that has been attributed to the relaxation of competition between rodents and large herbivores for food resources. To assess whether the removal of large herbivores also influenced a predator of small mammals, we measured the abundance of the locally common olive hissing snake, Psammophis mossambicus, over a 19-mo period in plots with and without large herbivores. Psammophis mossambicus was significantly more abundant in plots where large herbivores were removed and rodent numbers were high. Based on results from raptor surveys and measurements of vegetative cover, differences in snake density do not appear to be driven by differences in rates of predation on snakes. Instead, snakes appear to be responding numerically to greater abundances of small-mammal prey in areas from which large herbivores have been excluded. This is the first empirical demonstration of the indirect effects of large herbivores on snake abundance and presents an interesting example of how the influence of dominant and keystone species can move through a food web.     

Extremely high secondary production of introduced snails in rivers.

The functional importance of invasive animals may be measured as the degree to which they dominate secondary production, relative to native animals. We used this approach to examine dominance of invertebrate secondary production by invasive New Zealand mudsnails (Potamopyrgus antipodarum) in rivers. We measured secondary production of mudsnails and native invertebrates in three rivers in the Greater Yellowstone Area (Wyoming, USA): Gibbon River, Firehole River, and Polecat Creek. Potamopyrgus production was estimated by measuring in situ growth rates and multiplying by monthly biomass; native invertebrate production was estimated using size frequency and instantaneous growth methods. Mudsnail growth rates were high (up to 0.06 d(-1)) for juvenile snails and much lower for adult females (0.003 d(-1)). Potamopyrgus production in Polecat Creek (194 g x m(-2) x yr(-1)) was one of the highest values ever reported for a stream invertebrate. Native invertebrate production ranged from 4.4 to 51 g x m(-2) x yr(-1). Potamopyrgus was the most productive taxon and constituted 65-92% of total invertebrate productivity. Native invertebrate production was low in all streams. Based on a survey of production measures from uninvaded rivers, the distribution of secondary production across taxa was much more highly skewed toward the invasive dominant Potamopyrgus in the three rivers. We suggest that this invasive herbivorous snail is sequestering a large fraction of the carbon available for invertebrate production and altering food web function.     

Life history traits predict relative abundance in an assemblage of forest caterpillars

Species in a given trophic level occur in vastly unequal abundance, a pattern commonly documented but poorly explained for most taxa. Theoretical predictions of species density such as those arising from the metabolic theory of ecology hold well at large spatial and temporal scales but are not supported in many communities sampled at a relatively small scale. At these scales ecological factors may be more important than the inherent limits to energy use set by allometric scaling of mass. These factors include the amount of resources available, and the ability of individuals to convert these resources successfully into population growth. While previous studies have demonstrated the limits of macroecological theory in explaining local abundance, few studies have tested alternative generalized mechanisms determining abundance at the community scale. Using an assemblage of forest moth species found co-occurring as caterpillars on a single host plant species, we tested whether species abundance on that plant could be explained by mass allometry, intrinsic population growth, diet breadth, or some combination of these traits. We parameterized life history traits of the caterpillars in association with the host plant in both field and laboratory settings, so that the population growth estimate was specific to the plant on which abundance was measured. Using a generalized least-squares regression method incorporating phylogenetic relatedness, we found no relationship between abundance and mass but found that abundance was best explained by both intrinsic population growth rate and diet breadth. Species population growth potential was most affected by survivorship and larval development time on the host plant. Metabolic constraints may determine upper limits to local abundance levels for species, but local community abundance is strongly predicted by the potential for population increase and the resources available to that species in the environment.     

Ecology of a corallivorous gastropod,<Emphasis Type="Italic"> Coralliophila abbreviata</Emphasis>, on two scleractinian hosts. I: Population structure of snails and corals

Despite their potential importance in structuring reef communities, invertebrate corallivores and their population structures are poorly understood. We found distinct differences in the population structures (length-frequency distribution and sex ratio) of the corallivorous gastropod Coralliophila abbreviata residing on two coral-host taxa, Montastraea spp. and Acropora palmata, in the Florida Keys. In each of two survey years, around 50% of the Montastraea spp. colonies were infested, with a mean snail density of eight snails per infested colony (range 1–45), while around 20% of A. palmata colonies harbored three snails per infested colony (range 1–23). Variation in patterns of snail occurrence was also observed within a host taxon. A. palmata occurred in low- and high-density stands (0.4 and 1 colony m^–2, respectively, at the initial survey) at different sites. Hurricane Georges struck the area in September 1998. When resurveyed in 1999, density of colonies in low-density stands had decreased by 75% to 0.1 colonies m^–2. This decrease was accompanied by a doubling in the proportion of colonies infested with snails (from 19% to 46%) and an increase in snail density per infested colony (from 3.7±3.3 SD to 5.4±4.6 SD) as snails apparently concentrated on surviving A. palmata. In contrast, sites with high density A. palmata stands (thickets) retained colony densities of about ~1 colony m^–2 among years, while snail infestation increased only from 9% to 14% of colonies surveyed and snail density essentially remained unchanged (from 2.7±1.8 to 2.9±1.9 snails per infested colony). Snails collected from Montastraea spp. were shorter than those from A. palmata in low-density stands and were longest on A. palmata in thickets. On both host taxa, female snails were longer than males. The sex ratio of snails on Montastraea spp. hosts was even (1:1), while that of snails on A. palmata was skewed (70% males). Factors that could explain observed differences in size structure and sex ratio between Coralliophila populations on the two coral host taxa include: differential susceptibility to predators, influence of host tissue nutritional quality and/or secondary metabolite content, and genetic differences (cryptic species). The host-specific characteristics of C. abbreviata populations imply that the impact of gastropods on reef communities will vary with the coral species composition.     

Individual- and Assemblage-Level Effects of Anthropogenic Sedimentation on Snails in Lake Tanganyika

Abstract:  Human impacts on aquatic biodiversity are often measured at the assemblage or community level, although it has been suggested that individual-level measures are more sensitive. We evaluated the effects of anthropogenic sedimentation on endemic snails in Lake Tanganyika, East Africa, by comparing assemblage-level (i.e., species richness, evenness, and abundance) and individual-level (i.e., frequencies of predation and parasitism, fecal organic content, life history) data between sediment-disturbed and reference sites. Previous studies have indicated that sedimentation kills snails and reduces mollusc diversity in this system, but we found little evidence of changes in species richness, evenness, or snail abundance at the levels of sedimentation recorded. In contrast, individual-level data revealed a variety of differences associated with sedimentation. Frequencies of shell scarring by predatory crabs and castration by parasitic trematodes were significantly lower at disturbed sites, indicating shifts in interspecific interactions. Snails ingested large amounts of inorganic sediments at disturbed sites, suggesting a reduction in food quality. In addition, sedimentation was associated with a large downward shift in size distribution within some species and reproduction at smaller size. These strong patterns in individual-level data contrast with the lack of effects at the assemblage level. We argue that incorporating individual-level measures will often enhance the sensitivity of impact surveys and may reveal effects of disturbance on important interspecific interactions.     

When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants

An important question in the study of biological invasions is the degree to which successful invasion can be explained by release from control by natural enemies. Natural enemies dominate explanations of two alternate phenomena: that most introduced plants fail to establish viable populations (biotic resistance hypothesis) and that some introduced plants become noxious invaders (natural enemies hypothesis). We used a suite of 18 phylogenetically related native and nonnative clovers (Trifolium and Medicago) and the foliar pathogens and invertebrate herbivores that attack them to answer two questions. Do native species suffer greater attack by natural enemies relative to introduced species at the same site? Are some introduced species excluded from native plant communities because they are susceptible to local natural enemies? We address these questions using three lines of evidence: (1) the frequency of attack and composition of fungal pathogens and herbivores for each clover species in four years of common garden experiments, as well as susceptibility to inoculation with a common pathogen; (2) the degree of leaf damage suffered by each species in common garden experiments; and (3) fitness effects estimated using correlative approaches and pathogen removal experiments. Introduced species showed no evidence of escape from pathogens, being equivalent to native species as a group in terms of infection levels, susceptibility, disease prevalence, disease severity (with more severe damage on introduced species in one year), the influence of disease on mortality, and the effect of fungicide treatment on mortality and biomass. In contrast, invertebrate herbivores caused more damage on native species in two years, although the influence of herbivore attack on mortality did not differ between native and introduced species. Within introduced species, the predictions of the biotic resistance hypothesis were not supported: the most invasive species showed greater infection, greater prevalence and severity of disease, greater prevalence of herbivory, and greater effects of fungicide on biomass and were indistinguishable from noninvasive introduced species in all other respects. Therefore, although herbivores preferred native over introduced species, escape from pest pressure cannot be used to explain why some introduced clovers are common invaders in coastal prairie while others are not.     

Pyrrolizidine alkaloids on three trophic levels – evidence for toxic and deterrent effects on phytophages and predators

Summary. Pyrrolizidine alkaloids (PAs) present a model system in the investigation of tritrophic interactions mediated by plant secondary compounds. However, their toxicity for insect herbivores has never been experimentally proven. Here, we demonstrate the toxic effects of a PA on growth and survival of the eri silk moth Philosamia ricini. In a feeding experiment, larvae of this generalist herbivore fed with an artificial PA diet gained weight significantly slower than control animals, and died as pupae. We suggest that derivatives of the ingested PA N-oxide damage developmental functions during metamorphosis. A tracer test with [¹⁴C]senecionine N-oxide revealed that the caterpillars lack adaptations that would prevent conversion of the chemical into the pro-toxic free base. In contrast, the PA adapted leaf beetle Longitarsus anchusae accumulates PAs as N-oxides. We tested the purpose of sequestration in this species as defence against predators. Through a series of prey choice experiments with three carabid predator species, chemically non-protected bark beetle pupae were chosen almost uniformly over L. anchusae pupae. In a following choice test with one of these predators, artificially PA-treated mealworm segments deterred the predator from feeding. Overall the study corroborates the immediate toxic effect of PAs on non-adapted herbivores and the protective effect that adapted insects may gain by sequestering them. It thereby underlines the potential for PAs to play a central role in multitrophic interactions between plants, phytophages and their predators.