Population-level variation in plant secondary chemistry,and the population biology of herbivores

Summary Modern population ecology is becoming increasingly spatially-explicit. For insect hervibores, spatial variation in plant quality is a critical component of distribution and abundance. We argue that populationlevel measurements of phytochemical variation among individual plants has not kept pace with recent developments in population ecology. With examples from our own work, we demonstrate the importance of spatial variation in plant chemistry for insect herbivores, and suggest that phytochemistry should play a central role in the development of any spatially-based ecological theory.     

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.     

Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry

Allocation of resources to growth and defense against herbivores crucially affects plant competitiveness and survival, resulting in a specific distribution of assimilates and defense compounds within plant individuals. Additionally, plants rarely experience stable environmental conditions, and adaptations to abiotic and biotic stresses may involve shifts in resistance to herbivores. We studied the allocation of phytochemicals in Brassica oleracea (Brussels sprouts) due to leaf age, drought stress and herbivore damage and assessed effects on two lepidopteran herbivores differing in diet breadth: the generalist Spodoptera littoralis and the specialist Pieris brassicae. Glucosinolates as secondary defense compounds and total nitrogen and carbon were quantified and linked to plant palatability, i.e., herbivore feeding preference. Herbivore responses were highly species-specific and partially related to changes in phytochemicals. Spodoptera littoralis preferred middle-aged leaves with intermediate levels of glucosinolates and nitrogen over young, glucosinolate and nitrogen rich leaves, as well as over old leaves, poor in glucosinolates and nitrogen. In contrast, P. brassicae preferred young leaves. Both species preferred severely drought-stressed plants to the well-watered control, although analyzed glucosinolate concentrations did not differ. Both S. littoralis and P. brassicae feeding induced an increase of indole glucosinolate levels, which may explain a reduced consumption of damaged plants detected for S. littoralis but not for P. brassicae. By revealing distinct, sometimes contrasting responses of two insect herbivores to within-plant and stress-mediated intraspecific variation in phytochemistry of B. oleracea, this study emphasizes the need to consider specific herbivore responses to understand and predict the interactions between herbivores and variable plants.     

Costs and benefits of territorial defense in wild golden lion tamarins,Leontopithecus rosalia

Summary The costs and benefits of territorial defense were examined in a group of five wild golden lion tamarins, Leontopithecus rosalia, at Poco d'Antas Biological reserve, Rio de Janeiro, Brazil. I examined the effects of both interference and exploitative competition between groups of tamarins by comparing their use of space, time budgets and foraging success in different contexts of intergroup interactions and in quadrats shared and not shared by other groups. Tamarins spent more time moving and vocalizing, and less time feeding, foraging, and resting during intergroup encounters than in non-encounter contexts. Irrespective of intergroup distance, the group spent more time in overlapping areas of the range periphery than expected on the basis of quadrat availability. In those areas, however, foraging success per unit of foraging effort was lower than in exclusive areas of the range center. This suggests that access to high payoff central areas depended on costly defense (by both interference and exploitation) of the range periphery. Time and energy invested by the resident group in territorial defense (1) increased the availability of food in the range center, and (2) minimized food loss to neighboring groups in the range periphery. These benefits are likely to justify the costs of defense for an animal which depends on easily-depletable food supplies, such as prey in microhabitats and small concentrations of fruits and nectar.     

Intraspecific variation in a predator affects community structure and cascading trophic interactions

Intraspecific phenotypic variation in ecologically important traits is widespread and important for evolutionary processes, but its effects on community and ecosystem processes are poorly understood. We use life history differences among populations of alewives, Alosa pseudoharengus, to test the effects of intraspecific phenotypic variation in a predator on pelagic zooplankton community structure and the strength of cascading trophic interactions. We focus on the effects of differences in (1) the duration of residence in fresh water (either seasonal or year-round) and (2) differences in foraging morphology, both of which may strongly influence interactions between alewives and their prey. We measured zooplankton community structure, algal biomass, and spring total phosphorus in lakes that contained landlocked, anadromous, or no alewives. Both the duration of residence and the intraspecific variation in foraging morphology strongly influenced zooplankton community structure. Lakes with landlocked alewives had small-bodied zooplankton year-round, and lakes with no alewives had large-bodied zooplankton year-round. In contrast, zooplankton communities in lakes with anadromous alewives cycled between large-bodied zooplankton in the winter and spring and small-bodied zooplankton in the summer. In summer, differences in feeding morphology of alewives caused zooplankton biomass to be lower and body size to be smaller in lakes with anadromous alewives than in lakes with landlocked alewives. Furthermore, intraspecific variation altered the strength of the trophic cascade caused by alewives. Our results demonstrate that intraspecific phenotypic variation of predators can regulate community structure and ecosystem processes by modifying the form and strength of complex trophic interactions.     

Genetic variation in the mangrove periwinkle Littorina angulifera

Twenty populatios of Littorina angulifera, inhabiting islands composed of the mangrove tree Rhizophora mangle, were assayed at an esterase locus to determine whether genetic differentiation was associated with distance between populations. It was predicted, on the basis of larval dispersal in this species, that genetic differentiation between populations on islands separated by long distances should be greater than those on islands located near each other. A chi0square test of homogeneity revealed significant differences in esterase gene frequencies among the 20 island populations. However, there was no association of distance between islands and genetic heterogeneity. In addition, a cline in gene frequency was found to be assiciated with latitude. Factors responsible for the observed pattern of heterogeneity at the esterase locus are discussed.     

Genetic variation in the eel: a critique

A number of papers have dealt with protein variation in samples of eels of the genus Anguilla from throughout the North Atlantic Ocean. Examination of these published data from the standpoint of observed electrophoretic variations as well as statistical comparisons with genetic models, suggests that most genetic inferences concerning eels have been unjustified.     

Spatial distribution of defense chemicals and markers and the maintenance of chemical variation

Exploring the spatial distribution of variation in plant secondary metabolites is critical for understanding the evolutionary ecology of biochemical diversity in wild organisms. In the present study, concentrations of foliar sideroxylonal, an important and highly heritable defense chemical of Eucalyptus melliodora, displayed strong, fine-scale spatial autocorrelation. The spatial patterns observed could promote associational effects on herbivore foraging decisions, which may influence the selection pressures exerted on sideroxylonal content. Multiple chemical traits have roles in certain eucalypt-herbivore interactions, and the spatial characteristics of the herbivore foraging environment are therefore determined by these different factors. We used a model of E. melliodora intake by common brushtail possums (Trichosurus vulpecula), based on the combined effects of two chemical traits, to explore this idea and found that the spatial patterns were different to those of sideroxylonal alone. Spatial genetic autocorrelation, examined using microsatellites, was strong and occurred at a fine scale, implying that restricted gene flow might allow genetic patches to respond to selection relatively independently. Local two-dimensional genetic autocorrelation, explored using a new heuristic method, was highly congruent with the pattern of local phenotypic variation observed for sideroxylonal, suggesting that the genetic variance underlying the sideroxylonal variation is similarly structured. Our results suggest that the spatial distribution of genetic and phenotypic variation could influence both the selective pressure imposed by herbivores on eucalypt defenses and the potential of populations to respond to natural selection. Spatial context should be considered in future studies of plant-herbivore interactions.     

Geographic variation in maternal investment: acidity affects egg size and fecundity in Rana arvalis

Environmental-stress-mediated geographic variation in reproductive parameters has been little studied in natural vertebrate populations outside the context of climatic variation. Based on life-history theory, an increase in the degree of environmental stress experienced by a population should lead to (1) a shift in reproductive allocation from fecundity to offspring quality, (2) stronger trade-offs between reproductive parameters, and (3) changes in the relationship between female phenotype and maternal investment. To test these predictions, we investigated geographic variation in maternal investment of moor frogs (Rana arvalis) in relation to breeding site acidity (pH 4-8). We found that mean egg size increased and clutch size and total reproductive output (TRO) decreased with increasing acidity among 19 Swedish moor frog populations. Tests for variation and co-variation in maternal investment and female size and age in 233 females from a subset of four acid origin (AO) and four neutral origin (NO) populations revealed that clutch size and TRO increased with female size in both acid and neutral environments. However, in AO populations, egg size also increased with female size, and clutch size and TRO with female age, whereas in NO populations, egg size increased with female age. The strength of the egg-size-clutch-size tradeoff tended to be stronger in AO than in NO females as expected if the former experience stronger environmental constraints. All in all, these results suggest that environmental acidification selects for investment in larger eggs at a cost to fecundity, imposes negative effects on reproductive output, and alters the relationship between female phenotype and maternal investment.     

Genetic variation and biochemical systematics in the marine bryozoan Alcyonidium mytili

For many years the taxonomic position of the marine ctenostome bryozoan Alcyonidium mytili Dalyell (1848) has been in doubt, with some authorities regarding it as being conspecific with A. polyoum (Hassall). We have set out to resolve this problem using enzyme electrophoresis to examine the genetics of the population structure in the two species. The results show beyond reasonable doubt that sympatric populations of the two species are indeed from quite separate and non-interbreeding gene pools. An examination of various allopatric populations shows a new species of A. mytili to exist sympatrically with the other at Langstone Harbour, Hampshire, England. This species can be readily distinguished on morphological as well as genetic ground. Samples of A. mytili from Guernsey also show substantial genetic differences from other populations examined. It is tentatively concluded that this population also represents a separate gene pool and consequently should be recognised as a third species of A. mytili.     

Genetic variation and covariation during larval and juvenile growth in Mercenaria mercenaria

Quantitative genetic variances and covariances were estimated for shell length of the hard clam Mercenaria mercenaria (L.) at three larval stages (prodissoconch I, 2 d and 10 d post-fertilization) in 1987 and in 1988 after ca. 9 mo of growth. At each sample interval additive genetic variance was a highly significant component of the total size variation. Narrow sense heritability estimates for shell length ranged between 0.58 (±0.10) for prodissoconch I and 1.08 (±0.29) for 2-d-old larvae. There was significant and positive genetic covariance in prodissoconch I and 2-d larval shell length which resulted in a highly significant genetic correlation (r _g=0.74) between these two traits. This covariance is not surprising since the prodissoconch I comprises the majority of the larval shell of a 2-d-old larvae. The genetic covariances between 2-d-old and 10-d-old larvae and between 10-d-old larvae and 9-mo-old juveniles were low and not significantly different from zero. These results indicate that there is substantial genetic variation for shell growth in M. mercenaria but this variation is not stable during development; the genetic variation in shell growth at one stage of development is not strongly related to the genetic variation in growth during other ontogenetic periods. In this study there were no evident constraints to natural selection for increased shell growth rate during development, which coupled with the high levels of genetic variation may suggest that in nature high rates of larval growth may not be normally subject to significant selective pressure.     

Urbanization affects stream ecosystem function by altering hydrology, chemistry, and biotic richness.

Catchment urbanization can alter physical, chemical, and biological attributes of stream ecosystems. In particular, changes in land use may affect the dynamics of organic matter decomposition, a measure of ecosystem function. We examined leaf-litter decomposition in 18 tributaries of the St. Johns River, Florida, USA. Land use in all 18 catchments ranged from 0% to 93% urban which translated to 0% to 66% total impervious area (TIA). Using a litter-bag technique, we measured mass loss, fungal biomass, and macroinvertebrate biomass for two leaf species (red maple [Acer rubrum] and sweetgum [Liquidambar styraciflua]). Rates of litter mass loss, which ranged from 0.01 to 0.05 per day for red maple and 0.006 to 0.018 per day for sweetgum, increased with impervious catchment area to levels of approximately 30-40% TIA and then decreased as impervious catchment area exceeded 40% TIA. Fungal biomass was also highest in streams draining catchments with intermediate levels of TIA. Macroinvertebrate biomass ranged from 17 to 354 mg/bag for red maple and from 15 to 399 mg/bag for sweetgum. Snail biomass and snail and total invertebrate richness were strongly related to breakdown rates among streams regardless of leaf species. Land-use and physical, chemical, and biological variables were highly intercorrelated. Principal-components analysis was therefore used to reduce the variables into several orthogonal axes. Using stepwise regression, we found that flow regime, snail biomass, snail and total invertebrate richness, and metal and nutrient content (which varied in a nonlinear manner with impervious surface area) were likely factors affecting litter breakdown rates in these streams.     

Bearded seal males perceive geographic variation in their trills

Geographic variation in animal vocalisations, ranging from micro- to macro-variations, has now been widely documented. These dialects can impair communication between separated groups or populations and thus may play a role in speciation processes. Although the existence of geographical variation has been already shown in some pinnipeds species, the extent to which individuals perceive it is poorly understood. Here, we studied this question in the bearded seal Erignatus barbatus, a species found across different arctic regions. As in other phocids, bearded seal males emit sophisticated acoustic displays while defending an aquatic territory during the breeding season. First, we used playbacks to demonstrate that the trill has a function in territorial defence. Second, we used synthetic trills from two distinct populations (Nunavut and Greenland), to show that bearded seal males perceived the geographic variation in the trills. Males from Greenland responded more strongly to trills from local males than those from a distant area (Nunavut). This study provides the first experimental evidence that phocid males can perceive geographic variation in their vocalisations. Acoustic analyses combined with playback experiments can help to identify distinct populations in bearded seals. This may then provide information on both strength and scale of breeding site fidelity in this and potentially other species.     

Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen

Optimal defense theories suggest that a trade-off between defense costs and benefits maintains genetic variation within plant populations. This study assessed the independent and interactive effects of genetic- and environment-based variation in aspen leaf chemistry on insect performance, preference, and defoliation. Gypsy moth larvae were released into screenhouses containing eight aspen genotypes growing with high and low levels of nutrient availability. Plant chemistry, defoliation, and larval growth rates varied in response to genotype, nutrient availability, and their interaction. Total phenolic glycoside concentrations were inversely correlated with patterns of larval preference and were the best predictor of larval performance and defoliation among genotypes. Low-nutrient trees were less heavily defoliated and afforded decreased larval growth rates compared with high-nutrient trees. Nutrient availability mediated the defense benefits of phenolic glycosides, as plant chemistry explained significantly less variation in defoliation in low- compared with high-nutrient trees (7% vs. 44% of variation explained). These results suggest that spatial and temporal variation in resource availability may influence the relative magnitude of defense benefits in plants. Environmental mediation of the defense costs and benefits likely leads to diversifying selection and may maintain genetic polymorphisms in chemical defense traits in plant populations.     

Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera)

There has now been an abundance of research conducted to explore genetic bases that underlie learning performance in the honey bee (Apis mellifera). This work has progressed to the point where studies now seek to relate genetic traits that underlie learning ability to learning in field-based foraging problems faced by workers. Accordingly, the focus of our research is to explore the correlation between laboratory-based performance using an established learning paradigm and field-based foraging behavior. To evaluate learning ability, selected lines were established by evaluating queens and drones in a proboscis extension reflex (PER) conditioning procedure to measure learning in a laboratory paradigm—latent inhibition (LI). Hybrid queens were then produced from our lines selected for high and low levels of LI and inseminated with semen from many drones chosen at random. The genetically diverse worker progeny were then evaluated for expression of LI and for preference of pollen and/or nectar during foraging. Foragers from several different queens, and which had resulted from fertilization by any of several different drone fathers, were collected as they returned from foraging flights and analyzed for pollen and nectar contents. They were subsequently evaluated for expression of LI. Our research revealed that pollen foragers exhibited stronger learning, both in the presence (excitatory conditioning) and absence (LI) of reinforcement. The heightened overall learning ability demonstrated by pollen foragers suggests that pollen foragers are in general more sensitive to a large number of environmental stimuli. This mechanism could contribute toward explanations of colony-level regulation of foraging patterns among workers.Communicated by R. Page     

Genetic variation among trait groups and apparent absence of close inbreeding in grey-crowned babblers

Summary The grey-crowned babbler, Pomastostomus temporalis, is a non-migratory species with delayed breeding and prolonged association of young with siblings and parents. Since these conditions are conducive to incestuous matings, we have studied allozymic variation in a population in southeastern Queensland, to evaluate the possibility of close inbreeding. Eight of 20 loci tested were polymorphic, with an average proportion of heterozygous loci individual of 9.4%. No deficiency of heterozygotes was found, indicating the absence of detectable inbreeding. Some mechanism that prevents inbreeding seems to be present.     

Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte)

Summary. Maize plants respond to caterpillar feeding with the release of relatively large amounts of specific volatiles, which are known to serve as cues for parasitoids to locate their host. Little is known about the genetic variability in such herbivore-induced plant signals and about how the emissions in cultivated plants compare to those of their wild relatives. For this reason we compared the total quantity and the qualitative composition of the odour blend among eleven maize cultivars and five wild Zea (Poaceae) species (teosinte), as well as among the offspring of eight Zea mays mexicana plants from a single population. Young plants were induced to release volatiles by mechanically damaging the leaves and applying oral secretions of Spodoptera littoralis (Lepidoptera: Noctuidae) caterpillars to the wounded sites. Volatiles were collected 7 h after treatment and subsequently analysed by gas chromatography. The total amounts of volatiles released were significantly different among maize cultivars as well as among the teosintes. Moreover, striking differences were found in the composition of the induced odour blends. Caryophyllene, for instance, was released by some, but not all varieties and teosintes, and the ratios among monoterpenes and sesquiterpenes varied considerably. The offspring of different mother plants of the Z. m. mexicana population showed some variation in the total amounts that they released, but the composition of the odour blend was very consistent within the population of this teosinte species. We discuss the ecological significance of these findings in terms of specificity and reliability of induced plant signals for parasitoids.     

Genetic analysis of shell-shape variation in Littorina saxatilis on an environmental cline

Three shell-shape parameters of Littorina saxatilis were measured and found to vary in a regular pattern with distance up an estuary. The translation rate of the shell increased, the rate of whorl expansion decreased and the circularity of the aperture decreased proceeding from the exposed shore to the protected shore. The genetic variance of these traits was estimated from the full-sib covariance and the motheroffspring covariance. The genetic variance of the translation rate and the circularity of the aperture was low in all populations, but the genetic variance of the rate of whorl expansion was high on the exposed shore and low on the protected shore. It is argued that the change in mean phenotype of these traits is the result of natural selection produced by varying degrees of wave action and desiccation. The observed genetic variance is consistent with the theory that a trait under selection will show little additive genetic variance.     

Genetic variation in marine teleosts: High variability in habitat specialists and low variability in habitat generalists

Genetic variation was reviewed in 106 species of marine teleosts. Two heterozygosity estimates were used, one including all protein and enzyme loci and a second excluding the non-enzymatic protein loci. Mean heterozygosities are 0.055±0.036 based on all loci in 106 species and 0.060+0.038 based on enzymatic loci in 89 species. A significant negative correlation was noted between heterozygosity and the proportion of general protein loci included in the estimate. A comparison was made of heterozygosities among taxonomic orders and families, life zones, reproductive mode, geographical range and size. High levels of genetic variation are found in Clupeiformes, Atheriniformes, Pleuronectiformes, temperate pelagic, tropical, intertidal-sublittoral and wide-range species. Low levels of genetic variation are found in Gadiformes, Scorpaeniformes, temperate demersal, polar, and narrowrange species. The most striking differences in heterozygosities are between temperate demersal flatfishes and temperate demersal round fishes. It is suggested that much of the data can be explained by a habitat specialist-generalist model, with high heterozygosities in specialists and low heterozygosities in generalists, but that this is only one of a mosaic of factors which influence genetic variation.