Forest succession suppressed by an introduced plant-fungal symbiosis

Microbial symbionts can affect plant nutrition, defensive chemistry, and biodiversity. Here we test the hypothesis that symbionts alter the speed and direction of plant succession in communities that are shifting from grasslands to forests. A widespread C3 grass introduced to the United States, Lolium arundinaceum (tall fescue), hosts a fungal endophyte that is toxic to herbivores. In replicated experimental grasslands, the presence of the endophyte in tall fescue reduced tree abundance and size, altered tree composition, and slowed plant species turnover. In addition, consumption of tree seedlings by voles (Microtus spp.) was 65% higher in plots with the endophyte at the one grassland site where these data were collected. Despite its negligible contribution to community biomass, a microbial symbiont suppressed tree establishment, posing an important constraint on the natural transition from grasslands to forests.     

Host plant quality and local adaptation determine the distribution of a gall-forming herbivore

Herein we report results of transplant experiments that link variation in host plant quality to herbivore fitness at the local scale (among adjacent plants) with the process of local (demic) adaptation at the landscape scale to explain the observed distribution of the specialist gall former Belonocnema treatae (Hymenoptera: Cynipidae) within populations of its host plant, Quercus fusiformis. Field surveys show that leaf gall densities vary by orders of magnitude among adjacent trees and that high-gall-density trees are both rare (< 5%) and patchily distributed. B. treatae from each of five high-gall-density trees were reared on (1) the four nearest low-gall-density trees, (2) the four alternative high-gall-density trees, and (3) their natal trees (control). Each treatment (source X rearing site) was replicated three times. Nine components of performance that sequentially contribute to fitness were evaluated with over 21000 galls censused across the 25 experimental trees. When reared on their natal trees and compared with low-gall-density neighbors, transplanted gall formers had higher gall initiation success (P < 0.05), produced more (P < 0.001) and larger galls (P < 0.001), and produced a higher proportion of galls that exceeded the threshold size for natural enemy avoidance (P < 0.05). Comparison of gall-former performance on natal vs. alternative high-gall-density trees demonstrated significant (P < 0.001) differences in six performance measures with five differing in the direction predicted by the hypothesis of local adaptation. Overall, these linked experiments document direct and indirect effects of host plant variation on gall-former performance and demonstrate convincingly that (1) high-gall-density trees equate to high-quality trees that are surrounded by trees of relatively lower quality to the herbivore and (2) gall-former populations have become locally adapted to individual trees.     

Herbivory mediates grass-endophyte relationships

Endophytic fungi are plant symbionts living asymptomatically within plant tissues. Neotyphodium spp., which are asexual vertically transmitted systemic fungal endophytes of cool-season grasses, are predicted to be plant mutualists. These endophytes increase host plant resistance to environmental stresses and/or increase the production of alkaloid-based herbivore deterrents. The ubiquity of this defense mutualism is unclear, and a variety of alternative mechanisms may explain the observed variation in infection rates, levels of deterrence, and the maintenance of asexual endophytes in grass populations. We found that grass-endophyte interactions are variable and ordered along an herbivory gradient in an undisturbed subarctic alpine ecosystem. Native grass populations in grazed sites had significantly greater frequency of Neotyphodium infection compared to ungrazed sites. Tillers from grazed sites had significantly higher hyphal densities compared to ungrazed sites. The ability of grass-Neotyphodium constituents to deter vertebrate herbivory in natural systems is thought to be rare. In grazed meadows, we showed that endophyte infection resulted in the deterrence of grazing by native vertebrate herbivores. However, the same herbivores did not distinguish between infected and uninfected grass harvested from ungrazed areas. These results demonstrate that the relationship between vertically transmitted endophytes and grasses in the alpine tundra vary greatly within populations. This may be based in part on defense mutualism and is consistent, under varying levels of herbivory, with the predictions of optimal defense theory.     

Fitness related diet-mixing by intraspecific host-plant-switching of specialist insect herbivores

Generalist insect herbivores may profit by feeding on a mixture of plant species that differ in nutritional quality. Herbivore performance can also be affected by intraspecific host plant variation. However, it is unknown whether conspecific plant individuals differ sufficiently to promote diet-mixing behavior in specialist herbivores. We experimentally tested this "specialist diet-mixing hypothesis" for specialist caterpillars (Chrysopsyche imparilis, Lasiocampidae) in a West African savanna. The caterpillars switched regularly between host tree individuals (Combretum fragrans, Combretaceae). To examine whether switching benefited caterpillar performance via diet-mixing, the caterpillars were reared either on leaves from several plant individuals (mixed diet) or on leaves from a single plant. The strongest effect of diet-mixing was found for fecundity, with females reared on a mixed diet laying significantly more eggs than sisters receiving a single-plant diet. In addition, a mixed diet decreased variability in egg size and increased the growth of second-instar caterpillars. Supplementary food choice experiments were conducted to assess a potential influence of lowered host quality (induced by herbivory) on caterpillar behavior; no such effect was found. By linking intraspecific host-switching behavior and herbivore performance, this study provides new information on the relevance of intraspecific plant variation for herbivorous insects.     

The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in <Emphasis Type="Italic">Acromyrmex</Emphasis> leaf-cutting ants

Cuticular hydrocarbon profiles are essential for nestmate recognition in insect societies, and quantitative variation in these recognition cues is both environmentally and genetically determined. Environmental cues are normally derived from food or nest material, but an exceptional situation may exist in the fungus-growing ants where the symbiotic fungus garden may be an independent source of recognition compounds. To investigate this hypothesis, we quantified the chemical profiles of the fungal symbionts of 18 sympatric colonies of Acromyrmex echinatior and Acromyrmex octospinosus and evaluated the quantitative variation of the 47 compounds in a multivariate analysis. Colony-specific chemical profiles of fungal symbionts were highly distinct and significantly different between the two ant species. We also estimated the relative genetic distances between the fungal symbionts using amplified fragment length polymorphism (AFLP) and correlated these with the overall (Mahalanobis) chemical distances between the colony-specific profiles. Despite the standardized laboratory conditions, the correlations were generally weak, but a statistically significant portion of the total variation in chemical profiles could be explained by genetic differences between the fungal symbionts. However, there was no significant effect of ant species in partial analyses because genetic differences between symbionts tend to coincide with being reared by different ant species. However, compound groups differed significantly with amides, aldehydes, and methyl esters contributing to the correlations, but acetates, alkanes, and formates being unrelated to genetic variation among symbionts. We show experimentally that workers that are previously exposed to and fed with the fungal symbiont of another colony are met with less aggression when they are later introduced into that colony. It appears, therefore, that fungus gardens are an independent and significant source of chemical compounds, potentially contributing a richer and more abundant blend of recognition cues to the colony “gestalt” than the innate chemical profile of the ants alone. Freddie-Jeanne Richard and Michael Poulsen contributed equally to this work.     

The patchiness of epifoliar fungi in tropical forests: host range, host abundance, and environment

Fungal symbioses affect the diversity, dynamics, and spatial patterns of trees in tropical forests. Their ecological importance is partly driven by their inherent patchiness. We used epifoliar fungi, a guild of common, benign, obligate, fungal symbionts of plants, as a model system to evaluate the relative importance of host phylogeny, host relative abundance, and microclimate on the three-dimensional distribution of plant-fungus symbioses. In parallel studies in rainforests in Panama and Australia, most epifoliar fungi were able to colonize several plant lineages but showed significant host preferences within the local plant community. More closely related plant species were not more likely to share fungal symbionts. Instead, fungal species were more likely to be shared by more abundant hosts, which supported a greater number and diversity of fungi. Environmental conditions strongly affected spatial distributions, with sites in the dark understory 2.5- to fourfold more likely to have epifoliar fungi than in the exposed forest canopy. In the understory, fungal incidence increased with canopy openness. Canopy trees supported only a subset of the fungal symbionts found in the understory, suggesting that adult trees are not reservoirs of these fungal symbionts for understory juveniles.     

Associations of plant fitness, leaf chemistry, and damage suggest selection mosaic in plant-herbivore interactions

The geographic mosaic theory of coevolution states that variation in species interactions forms the raw material for coevolutionary processes, which take place over large geographic scales. One key assumption underlying the process of coevolution in plant-herbivore interactions is that herbivores exert selection on their host plants and that this selection varies among plant populations. We examined spatial variation in the existence and strength of phenotypic selection on host plant resistance exerted by specialist herbivores in 17 archipelago populations of the perennial herb Vincetoxicum hirundinaria (Asclepiadaceae). In these highly fragmented populations, V. hirundinaria is consumed by the larvae of two specialist herbivores: the folivorous moth Abrostola asclepiadis and the seed predator Euphranta connexa. Selection imposed on host plants by these herbivores was examined by analyzing the associations between levels of herbivory, plant fitness, and contents of a number of leaf chemicals reflecting plant resistance to and quality for the herbivores. We found extensive spatial variation in the levels of herbivory and in plant fitness. More importantly, the impact of both leaf herbivory and seed predation on plant fitness varied among plant populations, indicating spatial variation in phenotypic selection. In addition, leaf chemistry varied widely among plant populations, reflecting spatial variation in plant quality as food for the herbivores. However, leaf compounds influenced folivory similarly in all the studied plant populations, and interestingly, some of the compounds were associated with the intensity of seed predation. Finally, some of the leaf compounds were associated with plant fitness, and the strength and direction of these associations varied among plant populations. The observed spatial variation in the strength of the interactions between V. hirundinaria and its specialist herbivores suggests a geographic selection mosaic. Because the occurrence and strength of spatial variation varied between the two specialist herbivores, our results highlight the importance of considering multiple enemies when trying to understand evolution of interactions between plants and their herbivores.     

There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth

One of the challenges to quantifying the costs and benefits of symbiosis is that symbionts can influence different components of host fitness. To improve understanding of the ecology of inherited symbionts, we developed general theory for a perennial host-hereditary symbiont interaction, in which symbionts can have independent and potentially opposing effects on host regeneration and survival. The model showed that negative effects on one component of fitness may be outweighed by positive effects on another, leading to a net positive impact of symbiosis on population growth. Model predictions depended on the availability of suitable patches, which influenced the relative contributions of survival vs. regeneration to host fitness. We then used experimental symbiont removal to quantify effects of a hereditary, fungal endophyte on a grass host. Endophyte presence strongly reduced host survival but increased regeneration. Application of the model revealed that negative effects on plant survival were overwhelmed by beneficial effects on regeneration, resulting in stable endophyte persistence at 100% frequency, consistent with field observations. Our work demonstrates the utility of a demographic perspective for predicting the dynamics of symbioses and supports the hypothesis that symbionts function as mutualists when host and symbiont fitness are coupled through vertical transmission.     

Learning and natal host influence host preference,handling time and sex allocation behaviour in a pupal parasitoid

The host choice and sex allocation decisions of a foraging female parasitoid will have an enormous influence on the life-history characteristics of her offspring. The pteromalid Pachycrepoideus vindemiae is a generalist idiobiont pupal parasitoid of many species of cyclorrhaphous Diptera. Wasps reared in Musca domestica were larger, had higher attack rates and greater male mating success than those reared in Drosophila melanogaster. In no-choice situations, na?ve female P. vindemiae took significantly less time to accept hosts conspecific with their natal host. Parasitoids that emerged from M. domestica pupae spent similar amounts of time ovipositing in both D. melanogaster and M. domestica. Those parasitoids that had emerged from D. melanogaster spent significantly longer attacking M. domestica pupae. The host choice behaviour of female P. vindemiae was influenced by an interaction between natal host and experience. Female P. vindemiae reared in M. domestica only showed a preference among hosts when allowed to gain experience attacking M. domestica, preferentially attacking that species. Similarly, female parasitoids reared on D. melanogaster only showed a preference among hosts when allowed to gain experience attacking D. melanogaster, again preferentially attacking that species. Wasp natal host also influenced sex allocation behaviour. While wasps from both hosts oviposited more females in the larger host, M. domestica, wasps that emerged from M. domestica had significantly more male-biased offspring sex ratios. These results indicate the importance of learning and natal host size in determining P. vindemiae attack rates, mating success, host preference and sex allocation behaviour, all critical components of parasitoid fitness. Electronic Publication     

Monoterpene chemodiversity of ponderosa pine in relation to herbivory and bark beetle colonization

Summary. Ponderosa pine, Pinus ponderosa Laws. (Pinaceae), forests in Arizona have suffered from a nine-year period of drought and bark beetle, Ips lecontei Swaine (Coleoptera: Scolytidae), outbreaks. Abiotic and biotic stress in ponderosa pine results in the induced synthesis of certain monoterpenes that may in turn affect bark beetle behavior and survival. In this study, we investigate whether induced monoterpene production could result in a different monoterpene composition that remains stored in the needles or the trunk resin of the tree. Needle and resin samples in addition to trunk cores were collected from ponderosa pines at three locations in Arizona. Ungulate browsing induced a significant increase in limonene (P=0.010) and in chemodiversity (P=0.009), a measure of the evenness of distribution among the monoterpenes present in needles. We compared the level of ‘stress’ of the trees by measuring the thickness of annual rings in living trees and those that were killed by bark beetles. Where drought occurred, the spacing of annual rings from the last 10 years of trees killed by bark beetles was significantly smaller (P=0.020) compared to living trees. There was no difference in the monoterpene composition between the core sections of closest spacing of annual rings (stressed years) compared to the sections of widest spacing, which indicates that monoterpenes are distributed evenly throughout the extended resin system. In the area where the degree of drought was less overall, none of the individual monoterpenes present in the resin was related to bark beetle killed trees. However, about half the living pines had resin in which one of the major monoterpenes (α-pinene, Δ³-carene, and limonene) was absent, and these trees had a lower monoterpene chemodiversity compared to trees killed by bark beetles. Trees with these three major monoterpenes, corresponding to the average relative proportion in living pines at that location, may sustain higher selection and colonization by bark beetles.     

Survival trade-offs between two predator-induced phenotypes in Pacific treefrogs (Pseudacris regilla)

In many organisms, specific predator species induce defensive phenotypes that are qualitatively different from the phenotypes induced by other predator species. This differential induction implies that there is no optimal phenotype that works best against all predators. However, few studies have actually tested the hypothesis that each predator-induced phenotype provides the highest survival rate in encounters with the predator that induced that phenotype. In this experiment, I reared Pacific treefrog (Pseudacris regilla) larvae with chemical cues from two different predators (bluegill sunfish and predaceous diving-beetle larvae), and without predator cues. The Pacific treefrog larvae in the three treatments differed in their morphology and foraging behavior. I then exposed tadpoles from each treatment to free-foraging predaceous diving beetles and bluegill sunfish. Tadpoles survived best when exposed to the predator whose cues they were reared with, and worst when exposed to the other predator. In both predator environments, the tadpoles reared in the nonpredator control treatment had intermediate survival between the two predator-induced groups. Thus, there is no generalized "antipredator" response to these predators; rather, there was a clear trade-off in survival abilities between the predators.     

An autoradiographic examination of carbon fixation, transfer and utilization in the Riftia pachyptila symbiosis

Riftia pachyptila, the giant vestimentiferan tubeworm from the East Pacific Rise, harbors abundant chemolithoautotrophic, sulfide-oxidizing bacteria in an internal organ, the trophosome. Several facts, such as the lack of a digestive system in the host, stable carbon isotope values and net carbon dioxide uptake all suggest that the tubeworms obtain the bulk of their nutrition from their symbionts. Using tissue autoradiography, we investigated the mode of nutritional transfer between symbionts and host, and the site of early incorporation of symbiont fixed-carbon in the host. Fast labeling in the trophosome clearly demonstrates that the symbionts are the primary site of carbon fixation. Appearance of label in some symbiont-free host tissues in as little as 15 min indicates that the symbionts release a significant amount of organic carbon immediately after fixation. The organic carbon is largely incorporated into specific, metabolically active host tissues such as fast-growing body regions in the trunk and plume, and into tube-secreting glands. In addition to immediate release of fixed carbon by the symbionts, there is evidence of a second possible nutritional mode, digestion of the symbionts, which is consistent with previous suggestions based on trophosome ultrastructure. Results suggest that symbiont-containing host cells migrate in a predictable pattern within trophosome lobules and that symbiont division occurs predominately in the center of a lobule, followed eventually by autolysis/digestion at the periphery of the lobule. Received: 1 July 1999 / Accepted: 30 December 1999     

Two herbivore-deterrent iridoid glycosides reduce the in-vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L

Summary. Many secondary plant compounds are involved in defense against both insect herbivores and pathogens. Two secondary plant compounds of Plantago lanceolata, the iridoid glycosides catalpol and its precursor aucubin, are well known for their deterrent effects on generalist and non-adapted specialist insect herbivores. We tested the effects of these compounds on the in-vitro growth of a specialist and generalist fungal pathogen of this host species. Two chemical forms of these iridoids were tested. The glycosides and their aglycones, the products of enzymatic conversion by specific $/Beta$-glucosidase enzymes. The glycosides enhanced growth of both the specialist fungus Diaporthe adunca and the generalist fungus Fusarium moniliforme var. subglutinans. The positive effect of these glycosides on the generalist fungus is in sharp contrast with the generally negative effects of these glysosides on generalist insect herbivores. The aglycones of aucubin and catalpol reduced the growth of the specialist fungus D. adunca, but, contrary to expectation, enhanced the growth of the generalist fungus F. moniliforme var. subglutinans. Effects of aucubin on D. adunca were stronger than effects of catalpol. This was true both for the growth stimulating effects of the glycosides and for the fungitoxic effects of the aglycones. We therefore expect that the effects of these iridoids in P. lanceolata on the specialist fungus will strongly depend on the ratio between catalpol and its precursor aucubin and the chemical form (glycoside or aglycone) in which these compounds are encountered by the fungus during growth. Our results suggest that iridoid glycosides in P. lanceolata can be used as defense against both herbivores and pathogens, but that their effects are highly specific with respect to the natural enemy species that is encountered. Received 11 April 2002; accepted 9 August 2002     

Ubiquitous eight-carbon volatiles of fungi are infochemicals for a specialist fungivore

An enormous variety of volatile substances are released in distinctive blends by fungal substrates that should be recognisable for fungivores. Certain compounds dominate in most of the fungal species. Fungal oxylipins as the eight-carbon volatiles are the most prominent. This raises the question whether such are specific enough to qualify as appropriate host cues for a fungivore. We could demonstrate differentiated responses of the fungivorous beetle Bolitophagus reticulatus to eight-carbon volatiles: Nine eight-carbon volatiles were identified with GC–MS from its host fungus Fomes fomentarius. 1-Octen-3-ol, 3-octanone and 3-octanol induced contrasting behaviour of beetles in olfactometer bioassays. Electroantennographic experiments investigating the beetle olfactory sense revealed distinguishable antennal responses. Moreover, their individual release from F. fomentarius fruiting bodies changes not only considerably, but also independently over successive stages of beetle colonisation. Concentrations of attractive and repellent eight-carbon volatiles correlate to frequency of beetles in the field and further substantiate their relevance as host cues. Our results show that a specialist fungivore is able to differentiate the most common eight-carbon volatiles of fungi to assess host quality. Key roles and marked similarities of fungal to plant oxylipins suggest a comparable importance of eight-carbon volatiles to fungivores as green leaf volatiles have to herbivores.     

Evolution of plant volatile production in insect-plant relationships

Summary The production of volatile secondary plant substances during the evolution of terrestrial plants is reviewed in regard to the defensive systems of plants to microorganisms and herbivores. Plant volatiles can be produced by both anabolic and catabolic processes. Although attraction of pollinators is a well-studied phenomenon, functions of volatiles range from excretion of waste products to the production of compounds attracting natural enemies of herbivores. During the evolution of the angiosperms a diversity of volatiles were selected to defend generative parts against microorganisms. Many of these allomones were related to or even identical with sex pheromones of insects. As a result flowers of angiosperms became utilized as a mating site. Consequently insects visiting flowers became involved in pollination, facilitating the steps from anemophily to entomophily. The efficiency of entomophily was increased because of nutritional rewards.An evolutionary scenario for the impact of plant volatiles on insects is presented and the role of volatile allomones in the establishment of plant-insect relationships is emphasized by (1) their strong antimicrobial properties, (2) strategies to protect symbiotic microorganisms, (3) their function as repellents and deterrents, (4) the use of volatile allomones as kairomones. These facts speak for an adaptation of insects to plant physiology and a limited importance of phytophagous insects in selection pressure upon plants. Herbivorous insects have realized specific adaptations to be able to discriminate between complex odour blends, but the utilization of chemical groups among insect taxa is different.The main theories on plant chemical defence do not discuss the impact of volatiles on host plant selection and may be apt to revision when pheromones, allomones, kairomones and synomones are not taken into account.     

Combining optimal defense theory and the evolutionary dilemma model to refine predictions regarding plant invasion

Optimal defense theory posits that plants with limited resources deploy chemical defenses based on the fitness value of different tissues and their probability of attack. However, what constitutes optimal defense depends on the identity of the herbivores involved in the interaction. Generalists, which are not tightly coevolved with their many host plants, are typically deterred by chemical defenses, while coevolved specialists are often attracted to these same chemicals. This imposes an "evolutionary dilemma" in which generalists and specialists exert opposing selection on plant investment in defense, thereby stabilizing defenses at intermediate levels. We used the natural shift in herbivore community composition that typifies many plant invasions to test a novel, combined prediction of optimal defense theory and the evolutionary dilemma model: that the within-plant distribution of defenses reflects both the value of different tissues (i.e., young vs. old leaves) and the relative importance of specialist and generalist herbivores in the community. Using populations of Verbascum thapsus exposed to ambient herbivory in its native range (where specialist and generalist chewing herbivores are prevalent) and its introduced range (where only generalist chewing herbivores are prevalent), we illustrate significant differences in the way iridoid glycosides are distributed among young and old leaves. Importantly, high-quality young leaves are 6.5x more highly defended than old leaves in the introduced range, but only 2x more highly defended in the native range. Additionally, defense levels are tracked by patterns of chewing damage, with damage restricted mostly to low-quality old leaves in the introduced range, but not the native range. Given that whole-plant investment in defense does not differ between ranges, introduced mullein may achieve increased fitness simply by optimizing its within-plant distribution of defense in the absence of certain specialist herbivores.     

Herbivore-induced "rent rise" in the host plant may drive a diet breadth enlargement in the tenant

Inter- and intraspecies variations in host plant traits are presumably involved in many host shifts by insect herbivores, and elucidating the mechanisms involved in such shifts has been a crucial goal in insect-plant research for several decades. Here we propose that herbivore-induced evolutionary increases in host plant resistance may cause oligophagous insect herbivores to shift to other sympatric plants as currently preferred host plants become increasingly unpalatable. We tested this hypothesis in a system based on the perennial herb Filipendula ulmaria (Rosaceae), whose herbivory defense has become gradually stronger due to prolonged selection by Galerucella tenella (Coleoptera: Chrysomelidae) herbivory in a boreal archipelago. We show that Galerucella gradually increases its use of the alternative host plant Rubus arcticus (Rosaceae) in parallel to gradually increased resistance in Filipendula. Our results imply that, by driving the evolutionary increase in Filipendula resistance, Galerucella is also gradually making the original host species more unpalatable and thereby driving its own host-breadth enlargement. We argue that such self-inflicted "rent rises" may be an important mechanism behind host plant shifts, which in turn are believed to have preceded the speciation of many phytophagous insects.     

Glucosinolates and other metabolites in the leaves of <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> from natural populations and their effects on a generalist and a specialist herbivore

Because many secondary metabolites in plants act as defense against herbivores it has been postulated that these compounds have evolved under selective pressure by insect herbivores. One explanation for the within-species variation in metabolite patterns in a particular species is that different populations are under selection by different herbivores. We tested this hypothesis, using Arabidopsis thaliana plants that originated from dune and inland areas. We analyzed Arabidopsis thaliana leaves using NMR spectroscopy and multivariate data analysis. Major differences in chemical composition were found in water-methanol fractions and were due to higher concentrations of sinigrin and fumaric acid in dune plants. Inland plants showed lower levels of glucose. Quantitative analysis of glucosinolates was performed with HPLC. Individual plants and populations demonstrated differences in glucosinolate composition and concentration. In growth chamber experiments, the generalist herbivore, Spodoptera exigua grew significantly better on the inland plants, while the specialist herbivore Plutella xylostella performed equally well on plants of both origins. Aliphatic glucosinolate as well as total glucosinolate concentrations negatively correlated with larval mass of Spodoptera exigua. No significant correlations, however, were found between larval mass of Plutella xylostella and glucosinolates in the leaves. A specialist and a generalist herbivore were responding differently to plant secondary chemistry, as was also found in several other studies. This is an important indication that differences in glucosinolate concentrations among populations may result from differential selection by different guilds of herbivores.     

Nutrient subsidies to belowground microbes impact aboveground food web interactions

Historically, terrestrial food web theory has been compartmentalized into interactions among aboveground or belowground communities. In this study we took a more synthetic approach to understanding food web interactions by simultaneously examining four trophic levels and investigating how nutrient (nitrogen and carbon) and detrital subsidies impact the ability of the belowground microbial community to alter the abundance of aboveground arthropods (herbivores and predators) associated with the intertidal cord grass Spartina alterniflora. We manipulated carbon, nitrogen, and detrital resources in a field experiment and measured decomposition rate, soil nitrogen pools, plant biomass and quality, herbivore density, and arthropod predator abundance. Because carbon subsidies impact plant growth only indirectly (microbial pathways), whereas nitrogen additions both directly (plant uptake) and indirectly (microbial pathways) impact plant primary productivity, we were able to assess the effect of both belowground soil microbes and nutrient availability on aboveground herbivores and their predators. Herbivore density in the field was suppressed by carbon supplements. Carbon addition altered soil microbial dynamics (net potential ammonification, litter decomposition rate, DON [dissolved organic N] concentration), which limited inorganic soil nitrogen availability and reduced plant size as well as predator abundance. Nitrogen addition enhanced herbivore density by increasing plant size and quality directly by increasing inorganic soil nitrogen pools, and indirectly by enhancing microbial nitrification. Detritus adversely affected aboveground herbivores mainly by promoting predator aggregation. To date, the effects of carbon and nitrogen subsidies on salt marshes have been examined as isolated effects on either the aboveground or the belowground community. Our results emphasize the importance of directly addressing the soil microbial community as a factor that influences aboveground food web structure by affecting plant size and aboveground plant nitrogen.     

Sociality reduces individual direct fitness in a communally breeding rodent,the colonial tuco-tuco (<Emphasis Type="Italic">Ctenomys sociabilis</Emphasis>)

In many social vertebrates, remaining in the natal group leads to at least short-term reductions in the direct fitness of philopatric animals. Among communally breeding rodents, the direct fitness costs of philopatry appear to increase as the frequency of successful natal dispersal decreases, suggesting a functional link between constraints on natal dispersal and the reproductive consequences of sociality. To explore this relationship empirically, I documented patterns of direct fitness among female colonial tuco-tucos (Ctenomys sociabilis), which are group-living subterranean rodents from southwestern Argentina. Demographic data suggest that successful natal dispersal is rare in this species, leading to the prediction that natal philopatry in C. sociabilis is associated with significant reductions in individual direct fitness. Using data obtained during 1996–2001, I compared the direct fitness of females that dispersed from their natal group and bred alone as yearlings to that of females that lived and bred in their natal group as yearlings. Philopatric yearlings reared significantly fewer young to weaning than did disperser (lone) yearlings. Although neither survival to a second breeding season nor the estimated lifetime number of pups reared to weaning differed between dispersal strategies, the annual direct fitness of group-living females was 23–40% less than expected, suggesting that philopatric animals experienced a substantial direct fitness cost by remaining in their natal group. These data yield important insights into the adaptive bases for group living in C. sociabilis and suggest that constraints on natal dispersal are an important factor favoring group living in this species.Communicated by J. Wilkinson