Does pollution influence small mammal diet in the field? A metabarcoding approach in a generalist consumer

Mammals are mainly exposed to trace metals (TMs) via consuming contaminated food. Several studies have demonstrated relationships between metal concentrations in food and in animal tissues. However, potential effects of TMs on feeding behaviour of wildlife have been poorly documented under field conditions, despite experimental evidence showing that food selection is impacted by resource contamination. Here, we test the hypothesis that the diet of a generalist rodent, the wood mouse (Apodemus sylvaticus), is altered by soil TM contamination in the field. Wood mice were sampled in spring and in autumn along a gradient of soil contamination in the surroundings of a former smelter located in northern France. Available resources in the field were inventoried, and the diet of the animals was analysed using DNA “metabarcoding.” We demonstrated that (a) relationship between the resource richness in the diet and their richness in the field was altered by soil metal contamination. Wood mice specialized their diet along the gradient of soil metal contamination for both plant and invertebrate resources in spring. We also showed that (b) preference for Salicaceae, a plant family accumulating metals, decreased when soil contamination increased. These results suggest that environmental TM pollution could act as a force modulating trophic interactions in terrestrial food webs, thereby affecting wildlife exposure to contaminants by trophic route.     

Fractal Dimension in Butterflies’ Wings: a novel approach to understanding wing patterns ?

The geometrical complexity in the wings of several, taxonomically different butterflies, is analyzed in terms of their fractal dimension. Preliminary results provide some evidence on important questions about the (dis)similarity of the wing patterns in terms of their fractal dimension. The analysis is restricted to two groups which are widely used in the literature as typical examples of mimicry, and a small number of unrelated species, thus implying the consideration of only a fraction of the wing pattern diversity. The members of the first mimicry ring, composed by the species Danaus plexippus (better known as the monarch butterfly), and the two subspecies Basilarchia archippus obsoleta (or northern viceroy) and Basilarchia archippus hoffmanni (or tropical viceroy), are found to have a very similar value for the fractal dimension of their wing patterns, even though they do not look very similar at first sight. It is also found that the female of another species (Neophasia terlootii), which looks similar to the members of the previous group, does not share the same feature, while the Lycorea ilione albescens does share it. For the members of the second group of mimicry related butterflies, the Greta nero nero and the Hypoleria cassotis, it is shown that they also have very close values for the fractal dimension of their wing patterns. Finally, it is shown that other species, which apparently have very similar wing patterns, do not have the same fractal dimension. A possible, not completely tested hypothesis is then conjectured: the formation of groups by individuals whose wing patterns have an almost equal fractal dimension may be due to the fact that they do share the same developmental raw material, and that this common feature is posteriorly modified by natural selection, possibly through predation.We sincerely acknowledge the invaluable help of Adolfo Ibarra Vázquez, senior curator of the Lepidopterous collection at the Instituto de Biología, Universidad Nacional Autónoma de México, and the comments made by two anonymous referees     

Is individual consistency in body mass and reproductive decisions linked to individual specialization in foraging behavior in a long‐lived seabird?

Individual specialization in diet or foraging behavior within apparently generalist populations has been described for many species, especially in polar and temperate marine environments, where resource distribution is relatively predictable. It is unclear, however, whether and how increased environmental variability – and thus reduced predictability of resources – due to global climate change will affect individual specialization. We determined the within‐ and among‐individual components of the trophic niche and the within‐individual repeatability of δ¹³C and δ¹⁵N in feathers and red blood cells of individual female southern rockhopper penguins (Eudyptes chrysocome) across 7 years. We also investigated the effect of environmental variables (Southern Annular Mode, Southern Oscillation Index, and local sea surface temperature anomaly) on the isotopic values, as well as the link between stable isotopes and female body mass, clutch initiation dates, and total clutch mass. We observed consistent red blood cell δ¹³C and δ¹⁵N values within individuals among years, suggesting a moderate degree of within‐individual specialization in C and N during the prebreeding period. However, the total niche width was reduced and individual specialization not present during the premolt period. Despite significant interannual differences in isotope values of C and N and environmental conditions, none of the environmental variables were linked to stable isotope values and thus able to explain phenotypic plasticity. Furthermore, neither the within‐individual nor among‐individual effects of stable isotopes were found to be related to female body mass, clutch initiation date, or total clutch mass. In conclusion, our results emphasize that the degree of specialization within generalist populations can vary over the course of 1 year, even when being consistent within the same season across years. We were unable to confirm that environmental variability counteracts individual specialization in foraging behavior, as phenotypic plasticity in δ¹³C and δ¹⁵N was not linked to any of the environmental variables studied.     

How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system?

Diverse pollinator assemblages may impose complex selection and thus limit specialisation to particular pollinators. Previous work has concentrated on how visitation rates of different pollinators vary in space and time and how pollinators may vary in efficiency. In this study I quantify variation in visitation rates and foraging behaviour of different insect types (1) in space and time and (2) in relation to variation in floral design (flower size and form) and floral display (number of open flowers) for the distylous clonal shrub Jasminum fruticans. Mean visitation rate showed a significant interaction between insect type and population for seven populations in one year, and between insect types and years for a single population over 3 years. There was also a significant interaction between insect type and population for the proportion of flowers visited. In general the number of visits was positively related to the number of open flowers in a patch, but analyses by insect type showed that this was only true for bee flies and butterflies. Short-tongued bees showed a positive relationship between visitation rate and the number of open flowers on the focal stem, and hawkmoths and butterflies made more visits to plants with larger flowers. Hawkmoths were the only insect type to show a positive relation between the number of flowers visited per foraging bout and flower size. The significant differences between different insect types in patterns of variation in visitation rates in response to floral design and display may act to diversify selection on floral traits, and thereby constrain specialisation of the plant to particular pollinators.     

Varying foraging strategies of Labridae in seagrass habitats: Herbivory in temperate seagrass meadows?

The diets of five species of Labridae in south-western Australia were examined to determine whether: (1) grazing of seagrass and epiphytic algae is a prominent feature of the food web within the deeper seagrass meadows of this temperate region; (2) levels of grazing differ among different seagrass systems; and diets differ among these closely-related species. Fish were collected seasonally from three seagrass habitats mainly comprising either Posidonia sinuosa, Posidonia coriacea or Amphibolis griffithii between the summer of 1996/97 and spring of 1997. Consumption of considerable amounts of algae and seagrass by Odax acroptilus and seagrass by Haletta semifasciata indicates that macrophyte grazing by fish is a component of the trophic dynamics of south-western Australian seagrass meadows. O. acroptilus and H. semifasciata were both omnivorous, feeding on a range of epifauna, infauna and flora, whereas Siphonognathus radiatus, Neoodax balteatus and Notolabrus parilus were carnivorous, feeding predominantly on motile epifauna, such as molluscs and crustaceans. The level of macrophyte grazing is likely to be underestimated in temperate offshore meadows of P. sinuosa and A. griffithii where omnivorous labrids, monacanthids and terapontids are abundant. Stable isotope data for O. acroptilus from the study region suggest that animal prey is more important to tissue maintenance than macrophyte material. Macrophytes may be grazed to acquire attached animal prey or for fulfilling energy requirements. Based on the distribution of prey, it appears that species in A. griffithii meadows forage within and below the seagrass canopy, whilst species in P. sinuosa meadows are likely to forage towards the basal area of this seagrass.     

Do house mice modify their foraging behaviour in response to predator odours and habitat?

Predator odours and habitat structure are thought to influence the behaviour of small mammalian prey, which use them as cues to reduce risks of predation. We tested this general hypothesis for house mice, Mus domesticus, by manipulating fox odour density via addition of fox scats and habitat via patchy mowing of vegetation, for populations in 15 × 15-m field enclosures. Using giving-up densities (GUDs), the density of food remaining when an animal quits harvesting a patch, we measured foraging behaviours in response to these treatments. Mice consistently avoided open areas, leaving GUDs two to four times greater in these areas than in densely vegetated patches. However, mouse GUDs did not change in response to the addition of fox scats, even immediately after fresh scats were added. There was no interaction between fox odour and habitat use. We then tested whether habituation to fox odours had occurred, by comparing the individual responses to scats of eight mice born into enclosures with fox scats to those of eight mice born into scat-free enclosures and five wild mice. In smaller enclosures, GUDs of trays with scats did not differ from GUDs of trays without scats for any treatment. We conclude that exposure to high levels of fox odours did not alter the foraging behaviour of mice, but that mice did reduce foraging in areas where habitat was removed, perceiving predation risk to be greater in these areas than controls. We suggest further that studies using the ‘scat-at-trap’ technique, which have shown avoidance of predator odours by mice and other small mammals, may overestimate the general avoidance of predator odours by free-living prey, which must forage with a constant background of predator odours.     

Are clinical parameters sufficient to model gait patterns in patients with cerebral palsy using a multilinear approach?

The aim of this study was to evaluate whether clinical parameters are sufficient using, a multilinear regression model, to reproduce the sagittal plane joint angles (hip, knee, and ankle) in cerebral palsy gait. A total of 154 patients were included. The two legs were considered (308 observations). Thirty-six clinical parameters were used as regressors (range of motion, muscle strength, and spasticity of the lower). From the clinical gait analysis, the joint angles of the sagittal plane were selected. Results showed that clinical parameter does not provide sufficient information to recover joint angles and/or that the multilinear regression model is not an appropriate solution.     

Diet composition and foraging success in generalist predators: Are specialist individuals better foragers?

Factors affecting individual diet specialization in generalist populations and the relationship between diet and foraging success remain poorly studied, particularly in terrestrial wide-ranging predators. We studied whether individual variations in diet in Montagu's harrier males (determined through a combination of direct foraging observations and pellet analysis) were associated with patterns of foraging habitat selection and foraging success of 12 radiotracked males during the breeding period. We found important differences in diet composition and breadth between individuals. Diet diversity was negatively related to hunting success: the most efficient individuals in terms of hunting success had the most specialized diet. This study also suggests an important role of individual foraging habitat selection in explaining individual diet, as the proportion of different prey types in the diet was associated with habitat composition within the home range, with higher proportion of those habitats that held higher abundances of their more frequent prey. This study thus provides evidence of individual diet specialization having a knock-on effect on foraging efficiency in a wide-ranging raptor and highlights the role of individual behaviour as a driving force of intra-population niche variation.     

Rehabilitating a biological notion of race? A response to Sesardic

The point Sesardic (Biol Philos 25: 143–162, 2010) makes about the possibility of distinguishing groups for which there is a lot of within-group variation is not sufficient to rehabilitate a biological concept of race. In this note, I sketch a number of issues that quickly arise once we delve more deeply into the relevant scientific knowledge, concepts, methods, and questions for inquiry.     

Is there genetic variation in the response to competition intensity in juvenile brown trout Salmo trutta?

Effects of intraspecific competition intensities on the relative performance (growth and movement) of juvenile brown trout Salmo trutta originating from nine different families were tested in tank experiments and in semi-natural streams. Both growth and movement differed consistently among families, indicating genetic variation in these traits. There were no significant interaction effects, however, between the intensity of competition and family origin on performance in either of the two experimental systems. Thus, genetic variation in response to competition intensity appeared to be limited in the population from which the juveniles used in this experiment originate.     

The three-dimensional flight of red-footed boobies: adaptations to foraging in a tropical environment?

In seabirds a broad variety of morphologies, flight styles and feeding methods exist as an adaptation to optimal foraging in contrasted marine environments for a wide variety of prey types. Because of the low productivity of tropical waters it is expected that specific flight and foraging techniques have been selected there, but very few data are available. By using five different types of high-precision miniaturized logger (global positioning systems, accelerometers, time depth recorders, activity recorders, altimeters) we studied the way a seabird is foraging over tropical waters. Red-footed boobies are foraging in the day, never foraging at night, probably as a result of predation risks. They make extensive use of wind conditions, flying preferentially with crosswinds at median speed of 38 km h(-1), reaching highest speeds with tail winds. They spent 66% of the foraging trip in flight, using a flap-glide flight, and gliding 68% of the flight. Travelling at low costs was regularly interrupted by extremely active foraging periods where birds are very frequently touching water for landing, plunge diving or surface diving (30 landings h(-1)). Dives were shallow (maximum 2.4 m) but frequent (4.5 dives h(-1)), most being plunge dives. While chasing for very mobile prey like flying fishes, boobies have adopted a very active and specific hunting behaviour, but the use of wind allows them to reduce travelling cost by their extensive use of gliding. During the foraging and travelling phases birds climb regularly to altitudes of 20-50 m to spot prey or congeners. During the final phase of the flight, they climb to high altitudes, up to 500 m, probably to avoid attacks by frigatebirds along the coasts. This study demonstrates the use by boobies of a series of very specific flight and activity patterns that have probably been selected as adaptations to the conditions of tropical waters.     

Temporary cyst formation in phytoplankton: a response to allelopathic competitors?

Competition among phytoplankton for limiting resources may involve direct or indirect interactions. A direct interaction of competitors is the release of chemicals that inhibit other species, a process known as allelopathy. Here, we investigated the allelopathic effect of three toxic microalgae species (Alexandrium tamarense, Karenia mikimotoi and Chrysochromulina polylepis) on a natural population of the dinoflagellate Scrippsiella trochoidea. Our major findings were that in addition to causing death of S. trochoidea cells, the allelopathic species also induced the formation of temporary cysts in S. trochoidea. Because cysts were not lysed, encystment may act as a defence mechanism for S. trochoidea to resist allelochemicals, especially when the allelopathic effect is moderate. By forming temporary cysts, S. trochoidea may be able to overcome the effect of allelochemicals, and thereby have an adaptive advantage over other organisms unable to do so.     

Fructose and uric acid as drivers of a hyperactive foraging response: A clue to behavioral disorders associated with impulsivity or mania?

Several behavioral disorders, including attention deficit hyperactivity disorder (ADHD), bipolar disorder, and aggressive behaviors are linked with sugar intake and obesity. The reason(s) for this association has been unclear. Here we present a hypothesis supporting a role for fructose, a component of sugar and high fructose corn syrup (HFCS), and uric acid (a fructose metabolite), in increasing the risk for these behavioral disorders. Recent studies have shown that the reason fructose intake is strongly associated with development of metabolic syndrome is that fructose intake activates an evolutionary-based survival pathway that stimulates foraging behavior and the storage of energy as fat. While modest intake may aid animals that would like to store fat as a protective response from food shortage or starvation, we propose that high intake of sugar and HFCS causes a hyperactive foraging response that stimulates craving, impulsivity, risk taking and aggression that increases the risk for ADHD, bipolar disease and aggressive behavior. High glycemic carbohydrates and salty foods may also contribute as they can be converted to fructose in the body. Some studies suggest uric acid produced during fructose metabolism may mediate some of these effects. Chronic stimulation of the pathway could lead to desensitization of hedonic responses and induce depression. In conclusion, a hyperactive foraging response driven by high glycemic carbohydrates and sugars may contribute to affective disorders.     

Host-parasitoid association and diffuse coevolution: when to be a generalist?

In host-parasitoid communities, hosts are subjected to selective pressures from numerous parasitoid species, and parasitoids may attack several host species. The specificity of host resistance and parasitoid virulence is thus a key factor in host-parasitoid coevolution. A continuum of strategies exists, from strict specificity to a generalist strategy. The optimal level of specificity may differ in host and parasitoid. I investigated the optimal level of resistance specificity using a model in which the host could be attacked by two parasitoid species, with variable levels of defense specificity. The fitness of a parasitoid attacking two host species with different levels of virulence specificity was also modeled. Finally, a fluctuating environment was simulated by introducing variable probabilities of encounters between antagonistic species over several generations. If the frequency of encounters with the antagonistic species is fixed, then both host and parasitoid gain from a strategy of exclusive specialization toward the most frequent antagonist. If the frequency of encounters fluctuates between generations, generalist host resistance and partially specialist parasitoid virulence are favored. Generalist host resistance may be considered to be a bet-hedging response to an unpredictable environment. This asymmetry in host-parasitoid coevolution may account for some of the genetic structures observed in the field for host-parasitoid associations.     

Does interspecific competition drive patterns of habitat use in desert bat communities?

Bodies of water are a key foraging habitat for insectivorous bats. Since water is a scarce and limiting resource in arid environments, bodies of open water may have a structuring effect on desert bat communities, resulting in temporal or spatial partitioning of bat activity. Using acoustic monitoring, we studied the spatial and temporal activity patterns of insectivorous bats over desert ponds, and hypothesised that sympatric bat species partition the foraging space above ponds based on interspecific competitive interactions. We used indirect measures of competition (niche overlap and competition coefficients from the regression method) and tested for differences in pond habitat selection and peak activity time over ponds. We examined the effect of changes in the activity of bat species on their potential competitors. We found that interspecific competition affects bat community structure and activity patterns. Competing species partitioned their use of ponds spatially, whereby each species was associated with different pond size and hydroperiod (the number of months a pond holds water) categories, as well as temporally, whereby their activity peaked at different hours of the night. The drying out of temporary ponds increased temporal partitioning over permanent ponds. Differences in the activity of species over ponds in response to the presence or absence of their competitors lend further support to the role of interspecific competition in structuring desert bat communities. We suggest that habitat use and night activity pattern of insectivorous bats in arid environments reflect the trade-offs between selection of preferred pond type or activity time and constraints posed by competitive interactions.     

Reproduction,foraging and the negative density–area relationship of a generalist rodent

While many species show positive relationships between population density and habitat patch area, some species consistently show higher densities in smaller patches. Few studies have examined mechanisms that may cause species to have negative density–area relationships. We tested the hypothesis that greater reproduction in edge versus interior habitats and small versus large fragments contributes to higher densities of white-footed mice (Peromyscus leucopus) in small versus large forest fragments. We also examined vegetation structure and foraging tray utilization to evaluate if greater reproduction was a result of higher food availability. There were greater number of litters and proportion of females producing litters in the edge versus interior of forest fragments, which may have contributed to greater population growth rates and higher densities in edge versus interior and small versus large fragments. Data on vegetation structure and giving-up densities of seeds in artificial patches suggest that food availability may be higher in edge versus interior habitats and small versus large fragments. These results, in an area with few or no long-tailed weasels, provide a distinct contrast to the findings of Morris and Davidson (Ecology 81:2061, 2000) who observed lower reproduction in forest edge habitat as a result of high weasel predation, suggesting that specialist predators may be important in affecting the quality of edge habitat. While we cannot exclude the potential contributions of immigration, emigration, and mortality, our data suggest that greater reproduction in edge versus interior habitat is an important factor contributing to higher densities of P. leucopus in small fragments.     

Older parents are less responsive to a stressor in a long-lived seabird: a mechanism for increased reproductive performance with age?

In many taxa, reproductive performance increases throughout the lifespan and this may occur in part because older adults invest more in reproduction. The mechanisms that facilitate an increase in reproductive performance with age, however, are poorly understood. In response to stressors, vertebrates release glucocorticoids, which enhance survival but concurrently shift investment away from reproduction. Consequently, when the value of current reproduction is high relative to the value of future reproduction and survival, as it is in older adults, life history theory predicts that the stress response should be suppressed. In this study, we tested the hypothesis that older parents would respond less strongly to a stressor in a natural, breeding population of common terns (Sterna hirundo). Common terns are long-lived seabirds and reproductive performance is known to increase throughout the lifespan of this species. As predicted, the maximum level of glucocorticoids released in response to handling stress decreased significantly with age. We suggest that suppression of the stress response may be an important physiological mechanism that facilitates an increase in reproductive performance with age.