Strategies in herbivory by mammals revisited: The role of liver metabolism in a juniper specialist (Neotoma stephensi) and a generalist (Neotoma albigula)

Although herbivory is widespread among mammals, few species have adopted a strategy of dietary specialization. Feeding on a single plant species often exposes herbivores to high doses of plant secondary metabolites (PSMs), which may exceed the animal's detoxification capacities. Theory predicts that specialists will have unique detoxification mechanisms to process high levels of dietary toxins. To evaluate this hypothesis, we compared liver microsomal metabolism of a juniper specialist, Neotoma stephensi (diet >85% juniper), to a generalist, N. albigula (diet ≤30% juniper). Specifically, we quantified the concentration of a key detoxification enzyme, cytochrome P450 2B (CYP2B) in liver microsomes, and the metabolism of α‐pinene, the most abundant terpene in the juniper species consumed by the specialist woodrat. In both species, a 30% juniper diet increased the total CYP2B concentration (2–3×) in microsomes and microsomal α‐pinene metabolism rates (4‐fold). In N. stephensi, higher levels of dietary juniper (60% and 100%) further induced CYP2B and increased metabolism rates of α‐pinene. Although no species‐specific differences in metabolism rates were observed at 30% dietary juniper, total microsomal CYP2B concentration was 1.7× higher in N. stephensi than in N. albigula (p < .01), suggesting N. stephensi produces one or more variant of CYP2B that is less efficient at processing α‐pinene. In N. stephensi, the rates of α‐pinene metabolism increased with dietary juniper and were positively correlated with CYP2B concentration. The ability of N. stephensi to elevate CYP2B concentration and rate of α‐pinene metabolism with increasing levels of juniper in the diet may facilitate juniper specialization in this species.     

Diet breadth of mammalian herbivores: nutrient versus detoxification constraints

Two hypotheses, nutrient constraints and detoxification limitation, have been proposed to explain the lack of specialists among mammalian herbivores. The nutrient constraint hypothesis proposes that dietary specialization in mammalian herbivores is rare because no one plant can provide all requisite nutrients. The detoxification limitation hypothesis suggests that the mammalian detoxification system is incapable of detoxifying high doses of similar secondary compounds present in a diet of a single plant species. We experimentally tested these hypotheses by comparing the performance of specialist and generalist woodrats (Neotoma) on a variety of dietary challenges. Neotoma stephensi is a narrow dietary specialist with a single species, one-seeded juniper, Juniperus monosperma, comprising 85–95% of its diet. Compared with other plants available in the habitat, juniper is low in nitrogen and high in fiber, phenolics, and monoterpenes. The generalist woodrat, N. albigula, also consumes one-seeded juniper, but to a lesser degree. The nutrient constraint hypothesis was examined by feeding both species of woodrats a low-nitrogen, high-fiber diet similar to that found in juniper. We found no differences in body mass change, or apparent digestibility of dry matter or nitrogen between the two species of woodrats after 35 days on this diet. Moreover, both species were in positive nitrogen balance. We tested the detoxification limitation hypothesis by comparing the performance of the generalist and specialist on diets with and without juniper leaves, the preferred foliage of the specialist, as well as on diets with and without α-pinene, the predominant monoterpene in juniper. We found that on the juniper diet, compared with the specialist, the generalist consumed less juniper and lost more mass. Urine pH, a general indicator of overall detoxification processes, declined in both groups on the juniper diet. The generalist consumed half the toxin load of the specialist yet its urine pH was slightly lower. Moreover, the generalist consumed significantly less of the treatment with high concentrations of α-pinene compared to the control treatment, while the specialist consumed the same amount of food regardless of α-pinene concentration. For both groups, urine pH declined as levels of α-pinene in the diet increased. The generalist produced a significantly more acidic urine than the specialist on the treatment with the highest α-pinene concentration. Our results suggest that in this system, specialists detoxify plant secondary compounds differently than generalists and plant secondary compounds may be more important than low nutrient levels in maintaining dietary diversity in generalist herbivores. Received: 5 May 1999 / Accepted: 14 November 1999     

Differential hepatic gene expression of a dietary specialist (Neotoma stephensi) and generalist (Neotoma albigula) in response to juniper (Juniperus monosperma) ingestion

Dietary specialization is thought to be rare in mammalian herbivores because of limitations of their detoxification system in processing large doses of a single type of plant secondary compound (PSC). Therefore, in order to specialize on a single species of plant, mammalian herbivores must have a highly efficient detoxification system for the particular types of PSCs they ingest. Using microarray technology, we looked at the expression of hepatic genes of a dietary specialist, Neotoma stephensi, and a sympatric generalist, Neotoma albigula, in response to diets containing different levels of one-seeded juniper (Juniperus monosperma). We found large between species differences in gene expression, as well as large within species differences when specialists fed a low juniper diet (25% juniper) were compared to specialists fed their ecologically relevant level of juniper (70% juniper). We also tested the hypothesis that the specialist relies on less costly phase I detoxification enzymes more than phase II compared to the generalist. Although we found that the specialist had higher cumulative as well as average expression of phase I versus phase II enzymes, the generalist had a similar pattern of expression for phase I versus phase II enzymes.     

Cytochrome P450 2B Diversity and Dietary Novelty in the Herbivorous, Desert Woodrat (Neotoma lepida)

Detoxification enzymes play a key role in plant-herbivore interactions, contributing to the on-going evolution of ecosystem functional diversity. Mammalian detoxification systems have been well studied by the medical and pharmacological industries to understand human drug metabolism; however, little is known of the mechanisms employed by wild herbivores to metabolize toxic plant secondary compounds. Using a wild rodent herbivore, the desert woodrat (Neotoma lepida), we investigated genomic structural variation, sequence variability, and expression patterns in a multigene subfamily involved in xenobiotic metabolism, cytochrome P450 2B (CYP2B). We hypothesized that differences in CYP2B expression and sequence diversity could explain differential abilities of woodrat populations to consume native plant toxins. Woodrats from two distinct populations were fed diets supplemented with either juniper (Juniperus osteosperma) or creosote bush (Larrea tridentata), plants consumed by woodrats in their respective desert habitats. We used Southern blot and quantitative PCR to determine that the genomic copy number of CYP2B in both populations was equivalent, and similar in number to known rodent copy number. We compared CYP2B expression patterns and sequence diversity using cloned hepatic CYP2B cDNA. The resulting sequences were very diverse, and clustered into four major clades by amino acid similarity. Sequences from the experimental treatments were distributed non-randomly across a CYP2B tree, indicating unique expression patterns from woodrats on different diets and from different habitats. Furthermore, within each major CYP2B clade, sequences shared a unique combination of amino acid residues at 13 sites throughout the protein known to be important for CYP2B enzyme function, implying differences in the function of each major CYP2B variant. This work is the most comprehensive investigation of the genetic diversity of a detoxification enzyme subfamily in a wild mammalian herbivore, and contributes an initial genetic framework to our understanding of how a wild herbivore responds to critical changes in its diet.     

Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores

Constraints on rates of detoxification and elimination of plant toxins are thought to be responsible for limiting dietary specialization in mammalian herbivores. This hypothesis, known as the detoxification limitations hypothesis, suggests that most mammalian herbivores are generalists to avoid overdosing on toxins from a single plant species. The hypothesis also predicts that the few mammalian specialists that exist should have adaptations for rapid detoxification and elimination of plant secondary compounds. We took a pharmacological approach to test whether specialists eliminate toxins from the bloodstream faster than generalists. We compared elimination rate and total exposure of alpha-pinene in closely related dietary specialist and generalist woodrats, Neotoma stephensi and N. albigula, respectively. Animals were orally gavaged with alpha-pinene, a plant secondary compound present in the natural diets of both woodrat species. We collected venous blood at 3, 6, 10, 15, and 20 min post-ingestion of alpha-pinene. Blood was analyzed for alpha-pinene concentration using gas chromatography. We found that specialist and generalist woodrats did not differ in elimination rates of alpha-pinene. However, specialists had lower exposure levels of alpha-pinene than generalists due to lower initial delivery of alpha-pinene to the general circulation. The levels of alpha-pinene detected in the bloodstream of specialists were 4.7-5.3x lower over all time intervals than generalists. Thus, specialists encounter a functionally lower dose of toxin than generalists. We suggest that the lower exposure level of specialist woodrats may be due to mechanisms in the gut that decrease toxin absorption. Regardless of mechanism, lower exposure to plant toxins may allow specialists to forage on diets with high toxin concentrations thereby facilitating dietary specialization.     

Woodrat (<Emphasis Type="Italic">Neotoma</Emphasis>) herbivores maintain nitrogen balance on a low-nitrogen,high-phenolic forage, <Emphasis Type="Italic">Juniperus monosperma</Emphasis>

The acquisition of adequate quantities of nitrogen is a challenge for herbivorous vertebrates because many plants are in low nitrogen and contain secondary metabolites that reduce nitrogen digestibility. To investigate whether herbivores maintain nitrogen balance on plant diets low in nitrogen and high in secondary compounds, we studied the effect of juniper (Juniperus monosperma) ingestion on the nitrogen balance of two species of herbivorous woodrats (Neotoma stephensi and N. albigula). These woodrat species feed on the foliage of juniper: N. stephensi is a juniper specialist, whereas N. albigula is a generalist that incorporates some juniper in its diet. Based on the nitrogen contents of the natural diets of these woodrats, we predicted that the generalist would be in negative nitrogen balance on a juniper diet whereas the specialist would not be affected. We found that both species of woodrat had low-nitrogen requirements (334.2 mg N/kg^0.75/day) and that a diet of 50% juniper did not result in negative nitrogen balance for either species. However, excretion patterns of nitrogen were altered; on the 50% juniper diet, fecal nitrogen losses increased ~38% and urinary nitrogen losses were half that of the control diet. The results suggest that absorption and detoxification of juniper secondary compounds may be more important for restricting juniper intake by the generalist than nitrogen imbalance.     

Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes

Herbivores with very plastic dietary requirements, or so-called generalist species, can include individuals that develop specialized feeding habits through their experience with local chemically-defended plants. Local specialization has important implications for understanding a variety of ecological and evolutionary dynamics. However, the extent to which individuals within a generalist species specialize on local plants and the consequences of such specialization remain poorly understood, especially in non-insect herbivores. To better understand this phenomenon, we determined the diet and food preferences of a generalist mammalian herbivore, the dusky-footed woodrat ( Neotoma fuscipes ), in two adjacent but distinct plant communities. Based on a combination of cafeteria trials and stable isotope analyses (δ¹³C and δ¹⁵N), our results indicate that woodrats display preferences for local plants and tend to avoid novel chemically-defended plants. Moreover, both methodologies support the conclusion that individual woodrats are dietary specialists restricting their diets to only a few (2-3) of the available plant species. In juniper woodland, woodrats prefer western juniper ( Juniperus occidentalis ), while less than one km away in mixed-coniferous forest, woodrats prefer incense cedar ( Calocedrus decurrens ). Both plants contain high levels of plant secondary compounds that require detoxification mechanisms within consumers. Therefore, preferences are likely indicative of underlying physiological adaptations that could promote further behavioral, physiological and ultimately genetic differences between woodrats in different habitats. This study provides additional evidence for local specialization and urges caution when using the term generalist to characterize feeding behaviors at the individual level.     

Changes in phytophagous insect host ranges following the invasion of their community: Long‐term data for fruit flies

The invasion of an established community by new species can trigger changes in community structure. Invasions often occur in phytophagous insect communities, the dynamics of which are driven by the structure of the host assemblage and the presence of competitors. In this study, we investigated how a community established through successive invasions changed over time, taking the last invasion as the reference. The community included four generalist and four specialist species of Tephritidae fruit flies. We analyzed a long‐term database recording observed numbers of flies per fruit for each species on 36 host plants, over 18 years, from 1991 to 2009. Community structure before the last invasion by Bactrocera zonata in 2000 was described in relation to host plant phylogeny and resource availability. Changes in the host range of each species after the arrival of B. zonata were then documented by calculating diversity indices. The flies in the community occupied three types of niches defined on the basis of plant phylogeny (generalists, Solanaceae specialist, and Cucurbitaceae specialists). After the arrival of B. zonata, no change in the host range of specialist species was observed. However, the host ranges of two generalist species, Ceratitis quilicii and Ceratitis capitata, tended to shrink, as shown by the decreases in species richness and host plant α‐diversity. Our study shows increased host specialization by generalist phytophagous insects in the field following the arrival of an invasive species sharing part of their resources. These findings could be used to improve predictions of new interactions between invaders and recipient communities.     

Cytochrome P450 diversification and hostplant utilization patterns in specialist and generalist moths: Birth,death and adaptation

Across insect genomes, the size of the cytochrome P450 monooxygenase (CYP) gene superfamily varies widely. CYPome size variation has been attributed to reciprocal adaptive radiations in insect detoxification genes in response to plant biosynthetic gene radiations driven by co‐evolution between herbivores and their chemically defended hostplants. Alternatively, variation in CYPome size may be due to random “birth‐and‐death” processes, whereby exponential increase via gene duplications is limited by random decay via gene death or transition via divergence. We examined CYPome diversification in the genomes of seven Lepidoptera species varying in host breadth from monophagous (Bombyx mori) to highly polyphagous (Amyelois transitella). CYPome size largely reflects the size of Clan 3, the clan associated with xenobiotic detoxification, and to some extent phylogenetic age. Consistently across genomes, families CYP6, CYP9 and CYP321 are most diverse and CYP6AB, CYP6AE, CYP6B, CYP9A and CYP9G are most diverse among subfamilies. Higher gene number in subfamilies is due to duplications occurring primarily after speciation and specialization (“P450 blooms”), and the genes are arranged in clusters, indicative of active duplicating loci. In the parsnip webworm, Depressaria pastinacella, gene expression levels in large subfamilies are high relative to smaller subfamilies. Functional and phylogenetic data suggest a correlation between highly dynamic loci (reflective of extensive gene duplication, functionalization and in some cases loss) and the ability of enzymes encoded by these genes to metabolize hostplant defences, consistent with an adaptive, nonrandom process driven by ecological interactions.     

Host specialization is ancestral in Torymus (Hymenoptera,Chalcidoidea) cynipid gall parasitoids

The host range of parasitoids varies greatly among species: Some only parasitize one to a few hosts (specialists), while others parasitize multiple species or a variety of host types (generalists). The direction of most host range shifts in parasitoid groups, that is from generalist to specialist or, alternatively, from specialist to generalist, is unknown. To explore the origin of host range shifts, we studied a clade within the genus Torymus (Hymenoptera, Chalcidoidea) that includes both generalist and specialist parasitoids of Cynipidae (Hymenoptera). We analysed the phylogenetic relationships of the species of Torymus on the basis of two gene fragments (cox1 and ITS2) of 246 specimens and performed an ancestral state reconstruction of the specialist/generalist trait. Our results revealed the following: (a) The ancestral state of this group of Torymus is specialist, with the generalist state evolving through a loss of specialization. (b) The species Torymus cyaneus and Torymus flavipes both have a strong genetic structure, suggesting the existence of different biological identities. (c) There has been a host plant shift in the lineage(s) leading to Torymus rubi and Torymus bedeguaris from galls on Quercus to those on Rosaceae. (d) The alien species Torymus sinensis and the native European species Torymus notatus are phylogenetically closely related. (e) Speciation within Torymus was likely associated with the diversification of their cynipid hosts, which itself was driven by the dramatic changes in climate and vegetation that occurred during the Miocene.     

The polyphagous plant pathogenic fungus Botrytis cinerea encompasses host-specialized and generalist populations

The host plant is often the main variable explaining population structure in fungal plant pathogens, because specialization contributes to reduce gene flow between populations associated with different hosts. Previous population genetic analysis revealed that French populations of the grey mould pathogen Botrytis cinerea were structured by hosts tomato and grapevine, suggesting host specialization in this highly polyphagous pathogen. However, these findings raised questions about the magnitude of this specialization and the possibility of specialization to other hosts. Here we report specialization of B. cinerea populations to tomato and grapevine hosts but not to other tested plants. Population genetic analysis revealed two pathogen clusters associated with tomato and grapevine, while the other clusters co-occurred on hydrangea, strawberry and bramble. Measurements of quantitative pathogenicity were consistent with host specialization of populations found on tomato, and to a lesser extent, populations found on grapevine. Pathogen populations from hydrangea and strawberry appeared to be generalist, while populations from bramble may be weakly specialized. Our results suggest that the polyphagous B. cinerea is more accurately described as a collection of generalist and specialist individuals in populations. This work opens new perspectives for grey mould management, while suggesting spatial optimization of crop organization within agricultural landscapes.     

An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.     

The Relative Contribution of Specialists and Generalists to Mistletoe Dispersal: Insights from a Neotropical Rain Forest

Mistletoes rely on birds for seed dispersal, but the presumed importance of mistletoe‐specialist frugivores has not been critically examined nor compared with generalist frugivores and opportunistic foragers. The contribution of these three groups was compared directly by quantifying bird visitation to fruiting mistletoe plants ( Oryctanthus occidentalis: Loranthaceae) at Barro Colorado Island, Panama, and by comparing these results with proportions calculated from other empirical studies of mistletoe visitation conducted elsewhere. After more than 100 h of timed watches, 23 bird species were recorded visiting eight heavily infected host trees ( Luehea seemannii: Tiliaceae). Eight of these species visited mistletoe, of which five (all tyrannids) consumed mistletoe fruit. Although two mistletoe specialist frugivores ( Tyrannulus elatus and Zimmerius vilissimus) removed most fruit (73%), more than a quarter was consumed by one generalist frugivore ( Mionectes oleagineus) and two opportunists ( Myiozetetes cayanensis and Myiozetetes similis). Post consumption behaviour varied: the specialists flew from mistletoe to mistletoe, the generalist rested in the subcanopy and understory, and the opportunists spent most time hawking insects and resting high in the canopy. Integrating these data with previous work, the dietary specialization, short gut passage rate and strict habitat preferences of mistletoe specialists suggests that their services relate primarily to intensification and contagious dispersal, while species with broader diets are more likely to visit uninfected trees and establish new infections. The presumed importance of mistletoe‐specialist frugivores was not supported and mistletoes are considered to be comparable to many other bird‐dispersed plants, relying on both specialist and generalist frugivores, while opportunists may be disproportionately important in long‐distance dispersal.     

Xenobiotic metabolism of plant secondary compounds in juniper (Juniperus monosperma) by specialist and generalist woodrat herbivores, genus Neotoma

Mammalian herbivores routinely consume diets laden with often-toxic xenobiotics, yet the manner in which mammalian herbivores detoxify these plant secondary compounds (PSC) is largely unknown. Theory predicts that specialists rely more heavily on functionalization pathways whereas generalists rely on conjugation pathways to metabolize PSC in their diet. We took a pharmacological approach to determine how a specialist (Neotoma stephensi) of juniper foliage (Juniperus monosperma) and a generalist (N. albigula) may process the same dietary PSC. We investigated the xenobiotic metabolizing enzymes of the specialist and generalist on a control diet and a low (25%) juniper diet. We also examined enzyme activities in the specialist on a high (70%) juniper diet. We assayed for cytochrome P450 concentration and biotransformation activities of three specific cytochrome P450 isozymes (CYP1A, CYP2B, CYP3A), NAD(P)H:quinone oxidoreductase, glutathione conjugation, sulfation and glucuronidation. Results provide partial evidence for the hypothesis in that the specialist and generalist consuming juniper at a level similar to their natural diet, differ in the level of conjugation enzyme activity with generalists having higher activity overall than specialists.     

Antipredator responses in Tetranychus urticae differ with predator specialization

The behavioural response of Tetranychus urticae to chemical cues from specialist predatory mites, Phytoseiulus persimilis, or generalist predatory bugs, Orius majusculus, on either bean or strawberry was studied in experimental arenas. Predators were placed on the leaf disc for 24 h and removed before T. urticae females were introduced. After 24 h, prey fecundity (number of eggs laid) and dispersal (number of prey drowned in the water barrier) were assessed. Chemical cues from the specialist predator resulted in reduced prey fecundity, significantly different from the generalist predator and control treatments. No interaction effect was found between plant species and prey fecundity, while significantly more eggs were laid on bean than on strawberry. Predator cues irrespective of predator specialization resulted in more prey dispersal than in the control. Findings emphasize the importance of specialization in the predator species complex for the degree and type of antipredator responses and resulting biological control.     

Diversity and novelty of the gut microbial community of an herbivorous rodent (Neotoma bryanti)

Mammalian herbivores host diverse microbial communities to aid in fermentation and potentially detoxification of dietary compounds. However, the microbial ecology of herbivorous rodents, especially within the largest superfamily of mammals (Muroidea) has received little attention. We conducted a preliminary inventory of the intestinal microbial community of Bryant’s woodrat (Neotoma bryanti), an herbivorous Muroidea rodent. We collected woodrat feces, generated 16S rDNA clone libraries, and obtained sequences from 171 clones. Our results demonstrate that the woodrat gut hosts a large number of novel microorganisms, with 96% of the total microbial sequences representing novel species. These include several microbial genera that have previously been implicated in the metabolism of plant toxins. Interestingly, a comparison of the community structure of the woodrat gut with that of other mammals revealed that woodrats have a microbial community more similar to foregut rather than hindgut fermenters. Moreover, their microbial community was different to that of previously studied herbivorous rodents. Therefore, the woodrat gut may represent a useful resource for the identification of novel microbial genes involved in cellulolytic or detoxification processes.     

Cannibalism and Intraguild Predation Among Phytoseiid Mites: Are Aggressiveness and Prey Preference Related to Diet Specialization?

We tested whether specialist and generalist phytoseiid mites differ in aggressiveness and prey choice in cannibalism and intraguild predation. Specialists tested were Galendromus occidentalis, Neoseiulus longispinosus, Phytoseiulus persimilis, and P. macropilis; tested were Amblyseius andersoni, Euseius finlandicus, E. hibisci, Kampimodromus aberrans, Neoseiulus barkeri, N. californicus, N. cucumeris, N. fallacis, and Typhlodromus pyri. Aggressiveness of cannibalistic females against larvae was not related to diet specialization except that highly aggressive species were exclusively generalists. Seldom to moderately cannibalizing species occurred in both generalist and specialist phytoseiids. In contrast to aggressiveness in cannibalism, generalists and specialists differed in aggressiveness in intraguild predation. Adult females of specialists were only slightly aggressive against heterospecific larvae, whereas adult females of all generalists except T. pyri were highly aggressive. Adult females of generalists were able to discriminate between con- and heterospecific larvae and preferentially consumed the latter when given a choice. Adult females of specialists except G. occidentalis showed no preference when given a choice between con- and heterospecific larvae. We conclude that aggressiveness in intraguild predation, species recognition and subsequent preferential consumption of heterospecifics when given a choice is common in generalist but not specialist phytoseiids. We discuss the evolutionary pathways that might have led to the difference between specialists and generalists in species discrimination.     

Larval feeding induced defensive responses in tobacco: comparison of two sibling species of <Emphasis Type="Italic">Helicoverpa</Emphasis> with different diet breadths

Plants respond differently to damage by different herbivorous insects. We speculated that sibling herbivorous species with different host ranges might also influence plant responses differently. Such differences may be associated with the diet breadth (specialization) of herbivores within a feeding guild, and the specialist may cause less intensive plant responses than the generalist. The tobacco Nicotinana tabacum L. is the common host plant of a generalist Helicoverpa armigera (Hübner) and a specialist H. assulta Guenée (Lepidoptera, Noctuidae). The induced responses of tobacco to feeding of these two noctuid herbivores and mechanical wounding were compared. The results showed that the feeding of the specialist H. assulta and the generalist H. armigera resulted in the same inducible defensive system, but response intensity of plants was different to these two species. Inductions of jasmonic acid (JA), lipoxygenase (LOX), and proteinase inhibitors (PIs) were not significantly different concerning these two species, but H. assulta caused the less intensive foliar polyphenol oxidase (PPO) increase, more intensive nicotine and peroxidase (POD) increases in tobacco than H. armigera. The defensive response of plant to herbivores with different diet breadth seems to be more complicated than we expected, and the specialist does not necessarily cause less intensive plant responses than the generalist.     

Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource

For reciprocal specialization (coevolution) to occur among floral visitors and their host plants the interactions must be temporally and spatially persistent. However, studies repeatedly have shown that species composition and relative abundance of floral visitors vary dramatically at all spatial and temporal scales. We test the hypothesis that, on average, pollen specialist bee species occur more predictably at their floral hosts than pollen generalist bee species. Taxonomic floral specialization reaches its extreme among species of solitary, pollen-collecting bees, yet few studies have considered how pollen specialization by floral visitors influences their spatial constancy. We test this hypothesis using an unusually diverse bee guild that visits creosote bush (Larrea tridentatd), the most widespread, dominant plant of the warm deserts of North America. Twenty-two strict pollen specialist and 80 + generalist bee species visit Larrea for its floral resources. The sites we sampled were separated by 0.5 to > 1450 km, and spanned three distinct deserts and four vegetation zones. We found that species of Larrea pollen specialist bees occurred at more sites and tended to be more abundant than generalists. Surprisingly, spatial turnover was high for both pollen specialist and generalist bee species at all distances, and species composition of samples from sites 1–5 km apart varied as much as repeat samples made at single sites. Nevertheless, the pattern of bee species turnover was not haphazard. As distance among sites increased faunal similarity of sites decreased. Faunal similarities among sites within 250 km of each other were generally greater than if randomly distributed over all sites (the null model). No single ecological category of species (widespread, localized, Larrea pollen specialist, floral generalist) accounted for this spatial predictability. Evidently, concordant local distribution patterns of many ecologically diverse species contribute to the non-random spatial pattern. The ecological dominance of creosote bush does not confer obvious ecological advantages to its specialist floral visitors. Spatial turnover is comparable to that found for bee guilds from other biogeographic regions of the world and is not therefore limited to those bee species that inhabit highly seasonal climates, such as deserts. Philopatry and differences in bloom predictability among sites are probably more important causes for spatial turnover of bee species than are interspecific competition for nest sites or floral resources.     

The importance of environmental heterogeneity and spatial distance in generating phylogeographic structure in edaphic specialist and generalist tree species of Protium (Burseraceae) across the Amazon Basin

Aim Edaphic heterogeneity may be an important driver of population differentiation in the Amazon but remains to be investigated in trees. We compared the phylogeographic structure across the geographic distribution of two Protium (Burseraceae) species with different degrees of edaphic specialization: Protium alvarezianum, an edaphic specialist of white‐sand habitat islands; and Protium subserratum, an edaphic generalist found in white sand as well as in more widespread soil types. We predicted that in the edaphic specialist, geographic distance would structure populations more strongly than in the edaphic generalist, and that soil type would not structure populations in the edaphic generalist unless habitat acts as a barrier promoting population differentiation. Location Tropical rain forests of the Peruvian and Brazilian Amazon, Guyana and French Guiana. Methods We sequenced 1209–1211 bp of non‐coding nuclear ribosomal DNA (internal transcribed spacer and external transcribed spacer) and a neutral low‐copy nuclear gene (phytochrome C) from P. subserratum (n = 65, 10 populations) and P. alvarezianum (n = 19, three populations). We conducted a Bayesian phylogenetic analysis, constructed maximum parsimony haplotype networks and assessed population differentiation among groups (soil type or geographic locality) using analysis of molecular variance and spatial analysis of molecular variance. Results The edaphic specialist exhibited considerable genetic differentiation among geographically distant populations. The edaphic generalist showed significant genetic differentiation between the Guianan and Amazon Basin populations. Within Peru, soil type and not geographic distance explained most of the variation among populations. Non‐white‐sand populations in Peru exhibited lower haplotype/nucleotide diversity than white‐sand populations, were each other’s close relatives, and formed an unresolved clade derived from within the white‐sand populations. Main conclusions Geographic distance is a stronger driver of population differentiation in the edaphic specialist than in the generalist. However, this difference did not appear to be related to edaphic generalism per se as adjacent populations from both soil types in the edaphic generalist did not share many haplotypes. Populations of the edaphic generalist in white‐sand habitats exhibited high haplotype diversity and shared haplotypes with distant white‐sand habitat islands, indicating that they have either efficient long‐distance dispersal and/or larger ancestral effective population sizes and thus retain ancestral polymorphisms. These results highlight the importance of edaphic heterogeneity in promoting population differentiation in tropical trees.