Volume 28, Issue 5

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Cytokines and Eco-immunology: Studying the signalling molecule of the immune system

Laura M. Zimmerman, Rachel M. Bowden and Laura A. Vogel Ecologist at work. Photo provided by authors

Animals face the constant threat of pathogens, and the immune system has evolved to combat this threat. Despite the obvious benefits of a strong immune response, we often observe great variation in the abilities of animals to mount an immune response. Eco-immunology is a field where scientists are concerned with figuring out why this variation occurs in natural populations. Eco-immunologists examine many aspects of the immune system, and in this review we discuss the applicability to eco-immunology of examining cytokines. Cytokines are the signaling molecule of the immune system and they form a complex network that controls virtually all types of immune responses. We also discuss potential ways to measure these cytokines.

Some functions of cytokines include directing cells to the site of infection, causing cells to multiply, and stimulating them to produce antibodies. Some cytokines work together to produce a certain immune response, while some actually cancel out the effect of other cytokines. Methods of measuring cytokines can look at aspects of cytokine production such as the total amount of a cytokine present in a sample, identify the cells that produce them, or examine gene expression of the cytokine. The method used is based on the type of question the eco-immunologist wants to answer.

Most of what we know about cytokines comes from studies in mice and humans and, currently, over 60 different cytokines have been identified in these species. Recently, more research has focused on cytokines in fish, birds, reptiles, and amphibians, and we know now that not all types of animals produce the same cytokines. Different types of animals also face different challenges in their environment. For example, the immune system of reptiles is affected by environmental temperature, while that of birds is less likely to be similarly affected. This could potentially impact the cytokine production of cold-blooded animals and, ultimately, their immune response to a pathogen. Understanding how cytokines work in this wider range of animals can provide important information to eco-immunologists about why immune responses in wild animals are not always kept at a high, constant level.

Image caption: Ecologist at work. Photo provided by authors

 

Scaling leaf respiration in a tropical forest.

Martijn Slot, Camilo Rey-Sánchez, Klaus Winter and Kaoru KitajimaPhoto provided by authors.

Plants respire to produce energy and building blocks for growth. A waste product of respiration is CO2. As temperature increases, more energy is needed to maintain cellular functions, and consequently, more CO2 is released back into the atmosphere. The flux of CO2 released by respiration to the atmosphere is almost as large as the opposite flux, in which photosynthesis takes up CO2 from the atmosphere, and almost a third of the total respiration flux comes from leaves. Quantifying leaf respiration in relation to temperature is thus important to estimate the carbon balance of forest ecosystems.

Tropical forests are an important contributor to the global carbon cycle, but their diversity and their height makes it difficult to measure respiration fluxes for all species. In this study we quantified respiration of leaves of 28 species of trees and lianas (woody vines) in the upper-canopy of a tropical forest in Panamá —making use of a construction crane to access the canopy— and we correlated respiration rates, and the sensitivity of respiration to short-term temperature change, to other leaf traits that are easier to measure. Using these trait-correlations and long-term temperature data at our study site, we predicted temperature-dependent respiration of the whole canopy from the behaviour of individual leaves.

In contrast to predictions from global datasets, leaf phosphorus was a stronger correlate of respiration than leaf nitrogen. The combination of leaf phosphorus content, photosynthetic capacity, and leaf mass per unit leaf area could explain 64% of the variation in respiration at a set temperature, while the sensitivity of respiration to short-term temperature changes could be predicted from the concentration of sugars and starch in leaves and the growth form of the species (trees versus lianas). Respiration scaled to the stand level from these traits was estimated to release 7.4 ton of carbon per hectare per year. Similar fluxes have been estimated for other tropical forests, suggesting that using correlations with easy to measure traits instead of tedious direct measurements of respiration may make it easier to predict carbon fluxes in tropical forests in relation to temperature at a larger spatial scale.

Image caption: Photo provided by authors.
This paper can be found online here.

 

Pushing the limits to tree height: succulent treetop leaves of coast redwood store water.

H. Roaki Ishii, Wakana Azuma, Keiko Kuroda Stephen C. SillettPhotograph provided by authors..

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Coast redwood is the only tree species with living individuals exceeding 100 m in height. The tallest living individual stands 115.76 m as of 2013. The physiological mechanisms underlying its incredible stature have recently been documented, and water supply to treetop leaves is a key factor limiting physiological function and height growth of tall trees. However, mechanisms may exist that maintain water status of leaves and thus sustain physiological function near the treetop where light availability for photosynthesis is highest. Here we show evidence of foliar water storage as a mechanism for maintaining physiological function of treetop leaves in coast redwood. We measured water-use properties and morpho-anatomical characteristics of coast redwood foliage near the wet, northern and dry, southern limits of its geographic distribution in California, USA. We found that capacity to store water and the amount of water stored in foliage both increase with increasing height and light availability, maintaining tolerance of leaves to water stress constant with height. The morphology and anatomy of treetop leaves indicate increasing capacity for water storage and decreasing reliance on water transport from roots. Treetop leaves of coast redwood absorb moisture via leaf surfaces and have the potential to store more than five times the daily water demand. In coast redwood, water storage in foliage, near the site of photosynthesis, may be an important physiological adaptation that maintains water status and helps overcome constraints on water supply. This may explain how the world’s tallest species solves the dilemma that water stress is highest near the treetop, where light availability for photosynthesis is highest, and continues to push the limits of tree height.

Image caption: Photograph provided by authors..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Chemical compounds in fruits defend against pests.

Susan R. Whitehead and M. Deane BowersSibaria englemani feeding on an immature infructescence of Piper sancti-felicis. Photo credited to Susan R. Whitehead.

 

Plants produce fruits primarily to attract fruit-feeding animals, who benefit plants by inadvertently transporting seeds to new sites. However, the same nutritional rewards produced in fruits to attract beneficial animals can also attract a variety of pests and pathogens, which feed on fruits without providing any service to the plant. In this study, we examined whether some of the natural chemical compounds produced in fruits function to defend plants against fruit pests and pathogens. We focused on the plant genus Piper, a diverse group of tropical plants. Many plants in this group produce complex mixtures of chemical compounds called amides. For example, amides are responsible for the spicy heat of black peppercorns, which are the dried fruits of Piper nigrum. Our results show that amides also serve an important role in fruit defense. Certain amides deterred feeding by an insect seed predator and also strongly reduced the growth rates of several strains of fruit-associated fungi. We tested a variety of individual amides and mixtures of amides, and all showed some bioactivity against insects and/or fungi, although the strength of the effects were variable depending on the specific mixture of compounds and species of fruit pest being tested. In addition, our results showed that certain amides interacted with each other when they occurred in combination, such that the effects of the amide mixtures could not be predicted by simply adding up the effects of the individual compounds present. In some cases, the compounds interacted synergistically, leading to a stronger than expected effect, and in other cases they interacted antagonistically, leading to a weaker than expected effect. Overall, this study provides new evidence of the importance of fruit chemistry in plant defense against fruit-feeding pests and also emphasizes the potential complexity of effects on pests when compounds are present in mixtures.

 

Image caption: Sibaria englemani feeding on an immature infructescence of Piper sancti-felicis. Photo credited to Susan R. Whitehead.
The article is available here.

 

Interlopers pay the rent in nitrogen rather than protection in an ant-plant.

Joyshree Chanam, M.S. Sheshshayee, Srinivasan Kasinathan, Amaraja Jagdeesh, Kanchan A. Joshi and Renee M. BorgesLay Summary Photograph Caption:  Ants on a young leaf outside an ant shelter or domatium. Photocredit: Joyshree Chanam.

Myrmecophytes are special plants with unusual interactions with ants. Such plants produce nesting shelters called domatia for ants and could also provide ants with liquid or solid food. These benefits to ants have traditionally been considered to be in exchange for protection services that the ants provide against herbivores. The production of domatia was considered to be a strong incentive for protective ants to reside within these plants. However, whether plants with domatia had greater reproductive success in terms of fruit set owing to the presence of domatia has been difficult to examine because myrmecophytes almost always produce domatia, and it is difficult to remove domatia from plants. However, in the unique myrmecophyte Humboldtia brunonis, found only in the Western Ghats of India, only some individuals bear domatia on some of their branches, each domatium formed by modified swollen and hollow internodes, while all individuals produce extrafloral nectar. Moreover, these domatia meant for protective ants are prone to interloping residents because they have a self-opening slit that allows access to the domatium interior. Consequently, domatia in H. brunonis are occupied not only by many ant species, of which only one provides protection against herbivores, but also by numerous other invertebrates, most unusually an arboreal earthworm, which has antagonistic interactions with ants. Earlier studies have established that domatia-bearing H. brunonis plants have greater fruit set, hence greater reproductive success, than those without domatia. We show that plant tissues near domatia received 17% and 9% of their nitrogen from the ants (protective and non-protective) and the earthworm respectively. We also demonstrate that the absorbed nutrients travelled to distant branches; hence, fruit set was not different between branches with and without domatia. This is the first study to demonstrate that non-protective interlopers in the domatia pay the rent by contributing to plant nutrition. This can explain why even before the establishment of a specialised protection-based symbiosis with ants, plants bearing domatia may be favoured because of the nutritional benefits provided by a motley set of domatia residents that could even include arboreal earthworms.

Image caption: Lay Summary Photograph Caption: Ants on a young leaf outside an ant shelter or domatium. Photocredit: Joyshree Chanam.
The article is available here.

 

Natural habitat loss and exotic plants reduce the functional diversity of flower visitors.

Ingo Grass, Dana G. Berens & Nina FarwigAn individual of the African honeybee (Apis mellifera scutellata) approaches a Yellow Everlasting (Helichrysum ruderale)..

Pollinating insects are declining worldwide. This is worrying, as many of the world’s flowering plant species depend on insect pollinators for reproduction. Although the number of different pollinator species (pollinator richness) has been shown to be important for pollination, functional complementarity among different pollinators may play an even greater role. Functional complementarity means that flower visitors differ in certain characteristics that affect their pollination effectiveness. For example, a pollinator with a long tongue (proboscis) is a better match for plants with deep flowers than a pollinator with a short proboscis. Overall, the maintenance of plant diversity depends on pollinator species differing in morphological or behavioural traits, or, in other words, on the ‘functional diversity’ of pollinators.

Global change is a likely reason for the worldwide pollinator decline. Two strong drivers of global change are the loss of natural habitat and invasions of native communities by exotic (usually anthropogenically introduced) plant species. We know that these drivers often negatively affect pollinator richness; yet, we know virtually nothing about their effects on pollinator functional diversity. However, declines in pollinator functional diversity may be even more drastic than declines in pollinator richness.

We investigated the functional diversity of insect flower visitors in a subtropical South African landscape. Our study region is greatly affected by natural habitat loss and exotic plant invasions. We investigated functional diversity of three morphological traits that greatly influence flower handling and pollination efficiency: proboscis length, proboscis diameter and body length. We found that increasing habitat loss and abundance of exotic plants clearly reduced the functional diversity of flower visitors. In some cases, diversity of the three traits was negatively affected by both drivers and in other cases by only one of the two drivers. Contrastingly, we found no evidence for a decline in richness of flower visitors with either habitat loss or exotic plant invasions.

Our study shows that natural habitat loss and exotic plant invasions threaten the functional diversity of flower visitor communities, and that negative effects may not be evident if we only focus on species richness of flower visitors. Moreover, losses in functional diversity were partly driver-specific. This means that we need to consider multiple threats to flower visitors in order to gain insights into possible consequences of global change for pollination. Overall, our understanding of the effects of global change on pollinators and ultimate consequences for plant reproduction may greatly benefit from functional trait-based approaches.

Image caption: An individual of the African honeybee (Apis mellifera scutellata) approaches a Yellow Everlasting (Helichrysum ruderale).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Does body mass convey a digestive advantage for large herbivores?.

Patrick Steuer, Karl-Heinz Südekum, Thomas Tütken, Dennis W. H. Müller, Jacques Kaandorp, Martin Bucher Marcus Clauss & Jürgen HummelGrévy´s Zebra (Equus grevyi). Photograph provided by authors.

In many ancient and present ecosystems around the world, assemblies of ungulates (a group of large herbivorous mammals) make use of the available plant matter; herbivore faunas of the ice-age (“Pleistocene mammoth steppe”) or of present African savannahs represent fascinating examples. Their members range from relatively small creatures like antelopes/deer over cattle or horses up to real “megaherbivores” like giraffes, rhinos and elephants.

It has long been debated how all these herbivores manage to co-exist in an area and how they share their common food resources. Body size is considered to be a key trait. It is thought that large animals have to rely on low quality food (because they cannot select for the best plant parts), but that at the same time this disadvantage is balanced by their higher capacity to digest plant food (due to the longer time the food stays in their guts, allowing gut microbes more time to digest plant cellulose).

Our project wanted to test to what extent such scenarios are true. Two samples of herbivores of a considerable range of body sizes (from goats/antelopes to African elephants) were available: The first (17 species, kept in a large zoo and several other institutions) was fed on a uniform food resource (grass hay), whereas the second (19 species) was selecting a natural diet (free-ranging herbivores of East Africa). A proxy from faecal material (faecal protein content, largely depending on the amount of microbial biomass built during the digestive process) was used to evaluate digestibility realized by the animals.

No dependence of digestibility (faecal protein) on body mass was found for the animals fed on the uniform diet (grass hay), while for the free-ranging animals, a considerable decrease in digestibility was found. The first result contradicts an advantage of large over small animals in digestive ability. The considerable decrease of digestibility with increasing body mass found in the free-ranging herbivores strongly indicates that large animals like elephants had to select a diet of considerably lower digestibility than smaller herbivores, and that this lower quality was not balanced by a higher digestive ability in large herbivores.

Image caption: Grévy´s Zebra (Equus grevyi). Photograph provided by authors.
This paper can be found online here.

 

Lifetime consequences of food protein-carbohydrate content for an insect herbivore.

Karl A. Roeder and Spencer T. BehmerCaterpillar. Photo provided by authors.

All animals eat to acquire nutrients. For herbivores, two particularly important nutrients are protein and digestible carbohydrates. However, protein and digestible carbohydrate content in plants is often highly variable – both within and between plants. Herbivores can overcome this variability because they have a strong ability to regulate their protein-carbohydrate intake by practising dietary self-selection. In some situations, though, herbivores may not be able to practise dietary self-selection. For example, predators might block access to certain plant tissues, or abiotic factors (e.g., drought) may limit the range of available protein and carbohydrates. Where this happens, herbivores will be forced to eat whatever is available. The effect of food protein-carbohydrate content has been studied in a number of different herbivores, especially in insect herbivores, but usually only over a short time period, and never over a herbivore’s entire lifetime. In this study we reared newly hatched caterpillars (the tobacco budworm, Heliothis virescens) on a range of diets that differed in their protein-carbohydrate (p:c) ratio; the diets used spanned p:c ratios that can be observed in plants that would normally be eaten by this caterpillar. We recorded larval survival, time to pupation, pupal mass, survival rates and time to eclosion (emergence from the pupa), and pupal body lipid content. Additionally, for each diet, we mated successfully eclosed males and females and measured egg production and viability. Our results suggest that larval performance may not be overly sensitive to food p:c ratio, except when this differs widely from the self-selected p:c ratio. However, as food protein-carbohydrate content becomes increasingly imbalanced relative to the self-selected p:c ratio, pupal performance, most notably eclosion success, decreases. Additionally, males are more sensitive than females to protein-carbohydrate imbalances. Finally, when food protein-carbohydrate effects are explored at the population level, by combining larval and pupal performance with reproductive output (to generate estimates of population size and generation time), it becomes clear that there is a specific p:c ratio that is functionally optimal, and that small deviations away from this optimal ratio can have strong negative repercussions.

Image caption: Caterpillar. Photo provided by authors..
This paper can be found online here.

 

Exploring the nutritional basis of starvation resistance in Drosophila melanogaster.

Kwang Pum Lee and Taehwan Jang Drosophila melanogaster under starvation. Photo courtesy of authors.

Hunger is the most common stress encountered by all animals living in natural conditions where food is often scarce. Those individuals that withstand starvation better are more likely to pass on their genes to the next generations. It is common sense that how long animals can live without food depends partly on how much energy is stored in their body, which is in turn determined by the amounts and types of nutrients in foods they have been eating. It is not yet clear whether it is the quantity or the blend of nutrients that really matters for animals facing extreme food shortages. In this study, we used Drosophila fruit flies to tackle this tricky issue. Flies were fed diets with varying concentrations and ratios of protein and carbohydrate before they were plunged into the state of hunger. We found that flies that were previously fed low-protein, high-carbohydrate diets survived starvation longer than those fed high-protein, low-carbohydrate diets. Against our expectation, the amount of calories and nutrients eaten by flies had little influence on their resistance to starvation. These results tell us that the dietary balance between ingested nutrients is more important than the mere sum of caloric intake for flies when fighting hunger. To understand what really goes on inside the bodies of starving flies, we carefully tracked how their body nutrient reserves changed during starvation. According to our results, flies preferentially utilized non-fat substrates in the body to support life during the early stage of starvation. But once these resources were used up, they switched to burn off body fats throughout the remaining period of starvation. Flies died of starvation when fat reserves were emptied. Collectively, this study highlights that the way that animals cope with starvation is basically a nutritional process. For this reason, any phenotypic or genetic changes in starvation responses should be understood in a nutritional context.

Image caption: Drosophila melanogaster under starvation. Photo courtesy of authors.
The article is available here.

 

Carbon and phosphorus linkages in Daphnia growth are determined by growth rate, not species or diet.

James M. Hood and Robert W. Sterner Daphnia. Photo credited to James Hood and Robert Sterner.

All living things require a unique combination of chemical elements to grow and reproduce; therefore, the chemical composition of organisms can provide clues about the life and history of individuals and species. For example, the phosphorus (P) content of invertebrate bodies is one trait used to explain invertebrate distributions across gradients of P (which varies widely among water bodies and commonly limits algal growth). Because a large proportion of the P in invertebrates is associated with biomolecules involved in growth, several authors have predicted that the P content of invertebrates (a snapshot of their past and, possibly, future demand for P) should be positively correlated with a species’ growth rate, sensitivity to P limitation of growth and hence, abundance. This linkage between P and growth has a strong biological basis, but there is mixed support for relationships between fitness and the simple measure of body P. This study shows that growth-P linkages are revealed when a more realistic measure of demand is used.

We measured the growth of seven Daphnia (water flea) species on algal diets with low and high phosphorus contents and used this information to test predictions about relationships among body P content, growth rate, and sensitivity to P limitation. Like several other studies, we did not find support for the predicted relationships among these traits. However, by using an alternative approach -examining the linkage between carbon (C) and P accumulation in juvenile growth- we did find support for the principle that the P requirements of growth creates a tradeoff between maximizing growth and minimizing susceptibility to growth depression on low P diets.

Our results indicate that examination of C and P linkages in growth can replace body P content in predicting P demand, competitive tradeoffs, and perhaps even the role of species in nutrient cycling. Furthermore, our new approach appears to work better under the constantly changing conditions of aquatic systems. We hope that the approach we identified can be used to better understand how biochemical linkages between elements influence organisms and shape elemental cycles.

Image caption: Daphnia. Photo credited to James Hood and Robert Sterner.
The article is available here.

 

Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range.

Sarah R. McCann, Lee A. Rollins, Simon C. Griffith & William A. ButtemerThe cane toad (Rhinella marina, formerly Bufo marinus) is a large toxic anuran from South and Central America, currently spreading through its introduced range in Australia. Our studies on a montane cool-climate population of this invasive species show that toads can acclimate to low temperatures after only a few hours exposure. That rapid acclimation enhances the toad’s invasion success, and may allow it to spread into cooler regions than have been predicted by previous bioclimatic models. Photograph by Matt Greenlees.

All around the world, invading species are causing problems for native ecosystems. In order to deal with the invaders, we need to know how far they are likely to spread in their invaded range. Several methods have been developed to do this, and one of the most accurate is to examine the range of climatic conditions that are available to the invader in its new home. In general, we expect invaders to be able to occupy only areas that have conditions fairly similar to those in which they usually live.

Sometimes, however, invaders have surprised us, by spreading into areas that we thought were unsuitable for them. For example, the large and highly toxic cane toad has colonized much of tropical Australia, including areas much more arid than its home in the rainforests of South and Central America. Cane toads are now also moving into areas of southeastern Australia that were thought to be too cold for them. How can this tropical amphibian survive in the high, cold Border Ranges region of northeastern new South Wales?

We measured the cane toad’s ability to function at low temperatures by catching toads and cooling them down, to assess the temperature at which a toad was unable to flip itself back over if placed on its back. As we expected, toads from higher colder areas were able to function at lower temperatures than toads from nearby warmer places. Remarkably, however, even a few hours of being kept at low temperatures improved a toad’s thermal tolerance. Cane toads can rapidly adjust their physiology to deal with cold conditions.

That ability to adapt to low temperatures suggests that cane toads may be able to spread even further in Australia than is predicted by current models. More generally, animals that can acclimate quickly to extreme conditions may be especially troublesome invaders, extending further than we ever thought possible.

Image caption: The cane toad (Rhinella marina, formerly Bufo marinus) is a large toxic anuran from South and Central America, currently spreading through its introduced range in Australia. Our studies on a montane cool-climate population of this invasive species show that toads can acclimate to low temperatures after only a few hours exposure. That rapid acclimation enhances the toad’s invasion success, and may allow it to spread into cooler regions than have been predicted by previous bioclimatic models. Photograph by Matt Greenlees.
The article is available here.

 

Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders.

Vincent Careau, Matthew E. Gifford & Peter A. BiroSlimy salamander. Photo provided by authors..

We all intuitively know that humans differ from each other in almost every aspect of their morphology (e.g., body mass), physiology (e.g., alcohol tolerance), and behaviour (e.g., shy vs. bold). Not surprisingly, these individual differences also exist – and are naturally interesting to study – within species of wild animals.

Individual differences are often viewed as the “raw” material on which natural selection can act, as individuals with certain variants of a given trait may survive and reproduce more than individuals with other variants. Individual variation itself can also be considered as the result of natural selection, as certain types of selection (correlational or balancing) can generate and maintain variation among individuals within populations.

Over the last ~30 years, evolutionary physiologists have studied individual variation in a variety of traits, including the standard (lowest) and maximal (highest) metabolic rate that can be expressed by ectotherms (i.e., “cold-blooded” animals). Standard and maximal metabolic rates are fundamental measures in ecology and evolution because they set the range of conditions within which animals can perform activities that directly affect Darwinian fitness. Several studies revealed that individuals of similar body mass show 1.5 to 3-fold differences in metabolic rate within a single population.

Although metabolism is typically measured at a constant temperature to eliminate this important source of variation, we intentionally measured standard and maximal metabolic rates from 10 to 25°C in wild-caught slimy salamanders. We found that individual differences persisted across this temperature range, but the magnitude of individual variation (expressed relative to the total phenotypic variation) was ~60% lower than regularly reported in studies conducted at a single temperature.

This result was somewhat expected because temperature introduces variation within individuals. Such variation within individuals has traditionally been overlook as it was considered as “noise” that obscures interesting differences among individuals. Yet, we have shown that part of this within-individual variation was due to differences in how individuals responded to changes in temperature.

These among-individual differences in thermal sensitivity represent additional raw material on which natural selection can act, and/or sources of adaptive (co)variation. Thus, our study reveals the importance of considering within-individual variation in these apparently co-adapted traits.

Image caption: Slimy salamander. Photo provided by authors..
The article is available here.

 

Maternal effects and warning signal honesty in eggs and offspring of an aposematic ladybird beetle.

Anne E. Winters, Martin Stevens, Chris Mitchell, Simon P. Blomberg & Jonathan D. BlountSeven-spotted ladybird. Photo provided by authors.

Eggs are often subject to intense predation. One parental strategy to deter predators is to produce eggs that are laced with noxious chemicals and are conspicuously coloured as a warning signal (known as aposematism). Ladybird eggs are yellow/orange and contain toxins known as alkaloids; these traits are believed to function in concert as visual signal and chemical defence respectively. However, it remains unclear whether such aposematic signals reveal the strength (rather than simply the existence) of chemical defences. Furthermore, additional functions of egg pigments and toxins could apply; in particular mothers might deposit such resources into eggs to aid the development of offspring, or to provide resources that could contribute to aposematic traits in offspring.

We bred seven-spot ladybird beetles in the laboratory, and then measured relationships between egg colouration (in terms of the colouration metrics ‘brightness’, ‘hue’, and ‘saturation’) and toxin concentrations (the alkaloids precoccinelline and coccinelline). We also measured relationships between egg levels of carotenoid pigments and egg colouration. Finally, for a subset of eggs that were allowed to develop and the offspring reared until adulthood, we measured relationships between the colouration of the wing cases (an aposematic signal) and body toxin concentrations. As expected, we found that egg colour saturation correlated positively with egg levels of carotenoid pigments. In addition, egg concentrations of precoccinelline were positively correlated with egg colour saturation and hue. However, there were no significant relationships between egg coccinelline concentration and any measure of egg colouration. In young adults of both sexes, wing case colour saturation was significantly correlated with egg saturation and hue. Finally, body concentrations of coccinelline were significantly correlated with wing case hue. These results suggest that the colouration of 7-spot ladybird eggs is a reliable signal of the strength of the chemical defences they contain, but in addition, maternal investment of pigments and toxins into eggs may serve to influence the reliability of aposematic signalling in resultant offspring.

Image caption: Seven-spotted ladybird. Photo provided by authors.
This paper can be found online here.

 

Confusing Females: Colour Differences May Make Female Butterflies Difficult for Males to Identify.

Lisa B. Limeri and Nathan I. Morehouse  Orange-and-black (left) and white-and-black (right) females of the Orange Sulfur butterfly, Colias eurytheme. Photo courtesy of authors.

The diversity of colour patterns in nature has long fascinated biologists. Particularly puzzling are cases where members of the same species are colored differently. Common examples of this phenomenon, known as color polymorphism, include human hair color and eye color. However, how and why different color forms are maintained in populations over long periods of time is often not well understood. In the Orange Sulfur butterfly, a common agricultural pest that feeds on alfalfa, females come in two different color forms: black-and-orange or black-and-white. Black-and-white females, called ‘albas’, produce their less colorful patterns by reducing the amount of pigmentation in their wings, a strategy which allows them to reinvest these resources in faster development and increased egg production. Biologists have suggested that this strategy comes at a cost to ‘alba’ females, because males prefer to mate with the black-and-orange females. However, although some evidence for a male mating bias against ‘alba’ females does exist, little is known about why males would discriminate against these females, especially considering their higher egg production ability. We evaluated the hypotheses that either 1) males find ‘alba’ females difficult to see in their natural environments, or 2) males experience difficulties telling ‘alba’ females apart from other black-and-white butterfly species that live in the same habitats. Using detailed information about the vision of these animals, we “viewed” ‘alba’ and non-‘alba’ females through male eyes using mathematical models of butterfly vision. We find mixed evidence for the idea that ‘alba’ females may be more difficult to see against common backgrounds. However, we do find that males should face challenges discriminating between ‘alba’ females and other white butterflies commonly found in their environment. This suggests that the difficulties associated with properly distinguishing ‘albas’ from other species may be one reason underlying male mate biases against these black-and-white females. Such mating biases may counteract the other advantages of being an ‘alba’ female. Thus, limitations to male visual abilities may be important in maintaining both female color forms in this butterfly.

Image caption: Orange-and-black (left) and white-and-black (right) females of the Orange Sulfur butterfly, Colias eurytheme. Photo courtesy of authors.
The article is available here.

 

How to blend in.

Sami Merilaita and Marina DimitrovaCatching blue tits. Photo provided by authors.

Background matching means that an animal blends into its background due to visual similarity between its colour pattern and the environment. Background-matching coloration is a common form of protective coloration that has evolved in a broad range of animals. Although the similarity between the colour pattern of an animal and its natural background can be measured in many different ways, from an ecological and evolutionary viewpoint it is the degree of similarity experienced by a natural predator of the animal that is important as it determines the detectability of the pattern and hence its protective value. We explored the relationship between similarity and detectability by testing how stepwise changes in similarity in geometry between prey colour pattern and the visual background are reflected in its detectability. We conducted a predation experiment using artificial prey items and backgrounds. As predators we used wild-caught birds, blue tits, which typically search for camouflaged prey items for food. We trained the birds to search for artificial prey items that each concealed a piece of peanut as reward. In the experiment each bird received twelve presentations of prey with body colour patterns that to different degrees resembled the background, and we recorded the time it took the birds to detect the prey items. We found that initially the relationship between similarity and detectability was not linear. Instead, for prey that had high background matching, similarity had a larger impact on detectability than for prey with lower background matching. Most animals live in visually variable environments, and we also investigated background matching in an environment consisting of two different backgrounds. Obviously a colour pattern cannot simultaneously resemble perfectly several different background patterns, and therefore maximisation of background matching in a variable environment is more problematic. We found that a colour pattern that was a compromise between the two different backgrounds did equally well as the prey pattern that matched perfectly one of the backgrounds and mismatched the other. In conclusion, close similarity is strongly favoured in a single background, but in a variable environment a compromise pattern that only loosely resembles both backgrounds can provide relatively good protection.

Image caption: Catching blue tits. Photo provided by authors.
The article is available here.

 

A close arrangement of insect olfactory cells improves discrimination of odour sources.

Muhammad Binyameen, Júlia Jankuvová, Miroslav Blaženec, Rastislav Jakuš, Liwen Song, Fredrik Schlyter & Martin N. AnderssonEuropean spruce bark beetle, Ips typographus (left), and field trapping site (right). Photo courtesy of Fredrik Schlyter and Júlia Jankuvová..

How does an insect find food and mates over a distance, avoiding nearby stale food, defence chemicals, and competitors? It has been suggested that a specific, very close arrangement of olfactory cells inside olfactory hairs helps insects to find attractive sources of odour that are in close proximity to unpleasant odours. If two cells detecting two different odours are located within the same hair (“co-localised” cells), the insect should in theory be able to more precisely determine whether the odours emanate from the same source or from two closely separated ones, as compared to if the cells were located further apart on the antenna. For example, when two odours are released from the same source, they will activate the co-localised cells at exactly the same time, while odours that emanate from different sources would activate the cells at slightly different time points, providing the brain with a different temporal response pattern.

We show that the close arrangement of olfactory cells in olfactory hairs improves discrimination of odour sources in an important forest pest, the bark beetle Ips typographus, under natural field conditions. This beetle coordinates mass-attacks on trees by using an aggregation pheromone, but some odours released from attacked trees reduce the pheromone attraction. A tree defence compound, cineole, is one such odour, and verbenone is another. The beetles use the latter compound to avoid trees in late attack phases with low nutritional value, and the two compounds reduce pheromone attraction to similar levels. The olfactory cells for cineole, but not those for verbenone, are found in the same olfactory hairs as the cells for an essential pheromone component.

We used this olfactory subsystem to test the beetle response to the two inhibitors when they were placed at different distances from the pheromone on traps in the field. Beetle trap catch increased at shorter distance between the pheromone and cineole sources than between the pheromone and verbenone sources, demonstrating a better olfactory acuity for odours that are detected in the same olfactory hairs. This finding is of general importance for understanding principles of form and functions of the insect olfactory sense and will help to inform the utilisation of inhibitors for forest protection against bark beetles.

Image caption: European spruce bark beetle, Ips typographus (left), and field trapping site (right). Photo courtesy of Fredrik Schlyter and Júlia Jankuvová.
The article is available here.

 

Variation in early life testosterone within a wild population of red deer.

Alyson T Pavitt, Craig A Walling, Alan S McNeilly, Josephine M Pemberton & Loeske E. B Kruuk Female red deer (Cervus elaphus) with calf on the Isle of Rum, Scotland.

The sex hormone testosterone is usually associated with male reproduction, but its effects are far broader than this. Concentrations can differ substantially between individuals, and whilst high levels can benefit males in the breeding season, they can also reduce survival by making animals of both sexes more vulnerable to parasites and disease. Most research in this area has focussed on adults so far, however we were interested in whether there were any effects of varying testosterone in juvenile animals. We measured testosterone in blood plasma collected from wild Scottish red deer calves across a 17 year period, as part of a long-running red deer study on the Isle of Rum. We were interested in whether the condition of either the mother or calf caused testosterone to differ between calves, and particularly whether this affected a calf’s chances of survival.

Despite calves being only around two days old, testosterone was already higher in males, although both sexes showed a striking decline across the first day of life which flattened off at low levels after 24 hours. Interestingly, male calves had lower testosterone if they were born in the years after an older brother than if they had an older sister or were a firstborn. This sibling effect could be mediated by the condition of the mother, as we know sons are more costly to raise than daughters in this population (male calves are born larger and suckle longer than females).

Whilst testosterone did not seem to relate to survival across all calves, firstborn males (a group particularly vulnerable to mortality) were less likely to survive their first year if their testosterone concentrations were above average. This suggests that a young deer’s testosterone concentration can negatively affect their survival, but that these effects are only apparent if they are already at a higher risk of death.

Image caption: Female red deer (Cervus elaphus) with calf on the Isle of Rum, Scotland.
The article is available here.

 

Lifespan in the wild: the role of activity and climate in bees.

Jakub Straka, Kateřina Černá, Lenka Macháčková, Monika Zemenová and Petr KeilSolitary bee Anthophora plumipes on flower; photo credit Pavel Krásenský (macrophotography.cz).

Animal lifespan is potentially constrained by a number of environmental and physiological factors (temperature, humidity, metabolic rate, oxidative stress, etc.). Many of these have been studied in controlled conditions, but little is known about what influences animal lifespan in the wild. We assessed in situ environmental predictors of lifespan of two solitary bee species: a pollen specialist Andrena vaga (Andrenidae) and a pollen generalist Anthophora plumipes (Apidae). These bees forage and care for their offspring in the nests, and thus it is possible to observe them daily during most of their lives. For both species we collected extensive data on length of life, activity patterns during life and on environmental conditions, such as temperature, precipitation, sunshine, and pollen availability.

We found that lifespan is driven both directly by climate and indirectly by climate-dependent activity patterns. Specifically, we found a strong negative relationship between proportion of active days and length of life, and this proportion was related to climate. Also, individuals active during warm and/or wet days lived longer. Surprisingly, precipitation was a more important determinant of lifespan than temperature. Timing of the first appearance at the site was also an important predictor of the bee lifespan. Individuals that first appeared closer to the end of season lived for a shorter time than individuals that appeared earlier. Unsurprisingly, the exact timing of this first appearance was correlated with seasonal climate (temperature and precipitation).

Our study presents evidence that, in the wild, lifespan is constrained by an interplay of physical activity, precipitation, temperature, and food availability, and that this happens over at least two temporal scales (daily and seasonal). Understanding these constraints is important from both basic and applied perspectives. For instance, the prominent relationship between climate, activity patterns and lifespan suggest that climate change will have a profound effect on ecosystem services (e.g. pollination) that are directly dependent on animal activity and length of life.

Image caption: Solitary bee Anthophora plumipes on flower; photo credit Pavel Krásenský (macrophotography.cz).
The article is available here.

 

Poor food quality for hosts lowers transmission potential of their parasites.

Rachel M. Penczykowski, Brian C. P. Lemanski, R. Drew Sieg, Spencer R. Hall, Jessica Housley Ochs, Julia Kubanek, and Meghan A. Duffy Daphnia dentifera host infected with the fungal parasite Metschnikowia bicuspidata. Photograph credit: Isabella Oleksy.

Consumers face wide variation in resource quality across habitats and through time. In this study, we focused on how the quality of food available to hosts affects the ability of parasites to infect and replicate within them. For instance, hosts that eat higher quality food might be more resistant to infection if they are in better overall condition or can meet nutritional demands of immune function. On the other hand, better fed hosts may provide more fuel for the parasite to use for its own growth. Food quality may also influence host growth or behaviour in ways that affect the probability of encountering parasites and becoming infected. To differentiate among mechanisms such as these, we manipulated resource quality (high quality green alga vs. low quality cyanobacterium) for a freshwater zooplankton host. The host becomes infected by accidentally ingesting spores of a fungal parasite while filter feeding. We hypothesized that hosts fed the lower quality resource would have slower growth, consume parasite spores at a lower rate (due to a known positive relationship between body size and feeding rate for this species), and consequently have lower infection risk. In addition, we expected that the production of new parasite spores would be lower in hosts fed low quality food. As hypothesized, hosts on the low quality diet had low infection risk because of their small size and low rate of parasite exposure. Smaller hosts also yielded fewer parasite spores. However, there was also an effect of food quality on foraging behaviour independent of body size, and hosts that were switched from high to low quality food at the time of parasite exposure had much lower feeding rate and corresponding infection risk than expected for their body size. In a second experiment, we tested chemical traits of the low quality resource which might have driven these effects. Our study highlights that changes in food quality can alter multiple traits of hosts and parasites, and illustrates how those mechanisms can be experimentally disentangled. This is especially relevant for freshwater ecosystems, where excess nutrient loading often causes shifts from green algae to cyanobacteria.

Image caption: Daphnia dentifera host infected with the fungal parasite Metschnikowia bicuspidata. Photograph credit: Isabella Oleksy.
This paper can be found online here.

 

Community assembly and functional diversity along succession post-management

Radika Bhaskar, Todd E. Dawson, and Patricia BalvaneraTropical dry forest, Chamela Biological Reserve, Mexico. Photo by R. Bhaskar.

Ecologists have long been interested in whether plant communities recover in some predictable progression following a severe natural disturbance, such as a hurricane. Ecological theory suggests post-disturbance conditions are stressful, thus only the few species that can tolerate the harsh environmental filter will establish. With time, as conditions improve through recovery of vegetation and soil, a larger number of species can be supported, that then compete for resources.

The analysis of vegetation recovery takes on new urgency in light of extensive human modification, particularly in the tropics. Anthropogenic disturbance may not be analogous to ‘natural’ disturbance, and may change the pattern of recovery in unknown ways. Tropical dry forests (TDFs), characterized by seasonal drought, are experiencing unprecedented clearing. Though they have received much less scientific attention than wet forests, TDFs are important as habitat and for human welfare. Understanding how recovery proceeds post-management can aid in restoration efforts of this vulnerable and critical system.

Morphological characteristics of plants, or plant traits, can be used to assess responses to environmental conditions, to detect environmental filters and competition. We evaluated the recovery of a TDF in western Mexico following cattle ranching. We measured leaf and stem traits in plots recovering for 1 - 15 years after the ending of ranching and compared them to neighboring conserved TDF.

Forest recovery was only partially consistent with ecological theory. One leaf trait response indicated a progression from a narrow to a wider range of trait values, related to a transition from uniformly high light availability to dense shade, however the other two traits contradicted theoretical expectations. Analysis of a stem trait suggested water limits species establishment at all stages of recovery, and may be a resource particularly important in TDFs. Unexpected patterns not consistent with solely environmental or competitive processes may be a result of management legacy; individual adult trees exist in modified sites because farmers have kept them in pastures while clearing surrounding forests. In addition some TDF species can respond to clearing by resprouting, growing new stems from previous trunks or roots.

Our results suggest that to understand vegetation recovery post-management we need to take into account the influence of human interventions and the particularities of tropical dry forests.

Image caption: Tropical dry forest, Chamela Biological Reserve, Mexico. Photo by R. Bhaskar.
The article is available here.

 

Invasion and root heterogeneity.

Brenda M. Vaness, Scott D. Wilson and Andrew S. MacDougallPrairie crocus (Pulsatilla patens), a native species, is part of the diverse natural community lost following invasion by introduced grasses. Credit: S. Wilson.

Plant invasions are a widespread cause of global change. In North America, Eurasian grass species have invaded vast tracts of native prairie, altering wildlife habitat and producing species-poor “diversity deserts” that resist the reintroduction of native species.

We found that soil beneath invaded grasslands is consistently filled with roots. In contrast, soil beneath native prairie has more empty spaces that are available for invasive species to colonize. Overall, the patchiness of root length is about 30% lower beneath invaded grassland than native prairie.

Our results partly explain why native prairie is susceptible to invasion: soil beneath prairie has unoccupied spaces available for invaders to exploit. They also account for the difficulty of restoring native diversity to invaded grasslands: soil beneath the invaders is more fully occupied, leaving few opportunities for the reintroduction of native species.

Image caption: Prairie crocus (Pulsatilla patens), a native species, is part of the diverse natural community lost following invasion by introduced grasses. Credit: S. Wilson.
This paper can be found online here.

 

Epiphytes improve host plant water use by microenvironment modification.

Daniel Stanton, Jackelyn Huallpa Chávez, Luis Villegas, Francisco Villasante, Juan Armesto, Lars Hedin and Henry Horn Epiphytes such as these fog-soaked lichens can greatly change the microclimate of the host canopy in arid environments.

Epiphytes, plants that grow on other plants (including mosses, lichens, ferns and flowering plants) are often overlooked when we study forest ecology. Nonetheless, they can occur in very large quantities and researchers have shown them to contribute significantly to water and nutrient cycles in forests. Getting a clear picture of how much impact epiphytes can have is challenging: comparing trees with different epiphyte loads can confound factors (are the conditions different due to the differing amounts of epiphytes, or do the amounts of epiphytes differ because of conditions) and removing epiphytes involves difficult and dangerous tree-climbing.

However, not all epiphyte-covered trees are large. By working at two desert sites that receive large amounts of fog (one in northern Chile, one in southern Peru) we were able to strip epiphytes from naturally growing plants that were small (1-5m) and separate (so that overlapping canopies did not interfere). We removed either all of the epiphytes (from Caesalpinia spinosa trees in Peru) or half of the epiphytes (from the north or south-facing sides of Eulychnia spinosa cacti in Chile) and studied the effects of soil water and microclimate for the host. Furthermore, we complemented these experiments by constructing artificial cactus mimics that could be decked with epiphytes and studying soil moisture and microclimate in the absence of root water uptake and host transpiration.

Although we expected the epiphytes to increase the water inputs to the soil (by intercepting more fog that could then drip to the ground), we found the opposite: epiphytes held water in the canopy and decreased inputs to the soil. This water retention wasn't bad for the host though; plants with epiphytes took up soil water more slowly. This is explained by the epiphytes creating a significantly cooler and moister environment in the host plant canopy, with the potential to greatly reduce losses through transpiration. These results show that, at least in some ecosystems where epiphytes are abundant, epiphytes can have big impacts on the trees, and should be considered in models of forest ecosystem processes.

Image caption: Epiphytes such as these fog-soaked lichens can greatly change the microclimate of the host canopy in arid environments.
The article is available here.

 

Changing leaf nitrogen and canopy height quantify processes leading to plant and butterfly diversity loss in agricultural landscapes.

John G. Hodgson , Jerry Tallowinc, Roger L. H. Dennis , Ken Thompson, Peter Poschlod, Mewa S. Dhanoa, Mike Charles, Glynis Jones, Peter Wilson, Stuart R. Band, Amy Bogaard, Carol Palmer, Gaylynne Carter, Alison Hynd.The English countryside: a mosaic of farmed and unfarmed components. Photo provided by authors..

Agri-environment schemes that support wildlife friendly farming practices aim to counterbalance impacts of intensive agriculture on biodiversity in the countryside. Using England as an example, this paper attempts to quantify the effectiveness of these schemes not, in the traditional way, by identifying ‘winners’ and ‘losers’, but by examining the impact of key processes that determine the species composition of the countryside.

We compared three independent numerical measures for the English countryside: the farmer’s viewpoint (as identified by governmental agricultural statistics), the nature conservationist’s (using distribution atlases of plant and butterfly species) and the ecologist’s (using published functional traits of individual plant species to quantify their tolerance to changes in environmental variables such as soil fertility and frequency of management ).

We show that despite the implementation of agri-environment schemes and other conservation measures, diversity of native English plants remains strongly negatively correlated with agricultural intensity, as assessed from governmental agricultural statistics: heavily farmed English counties are disproportionately poor in species. Moreover, this lower biodiversity in the most intensively-farmed parts of England results from two separate processes. On farmland itself, the exclusion of slow-growing species of infertile soils, intolerant of ‘active’ management processes designed to boost crop yields (e.g. fertilizer additions and herbicide application to eliminate competition by weeds) was most complete in intensively farmed landscapes. However, much floristic diversity probably now resides (at least within arable regions) in unmanaged (or infrequently-managed) habitats outside the ‘working agricultural landscape’ (field margins, old quarries, track and roadsides) and here, associated with an increase in plant height, more ‘passive’ processes are at work. In these unmanaged parts of intensively farmed regions, tall species have been encouraged at the expense of shorter ones. Moreover, these continuing changes, both ‘active’ and ‘passive’, are not confined to plants. The butterflies considered most at risk of extinction feed, both as larvae and as adults, on slow- and low-growing food plants.

Analyses of this type can help improve conservation policies. For example, efficiency can be increased simply by integrating policies for conserving biodiversity within and outside farmland. Future improvements should be generated not, as in the past, by ‘learning from mistakes’ but by predicting and anticipating potential problems by reference to ecological and economic theory and through experimentation and data analysis.

Image caption: The English countryside: a mosaic of farmed and unfarmed components. Photo provided by authors..
The article is available here.

 

Meristem limitation explains lags in the response of productivity to changes in precipitation in arid grasslands.

Lara G. Reichmann and Osvaldo E. Sala Rainout shelter used in the rainfall manipulation experiment at the Jornada LTER. Dr. Reichmann (pictured) and Dr. Sala studied lags in the response of productivity to changes in precipitation.

Ecologists have assumed for a long time that arid and semiarid ecosystems are mostly limited by water availability. Surprisingly, the strong relationship between mean annual precipitation and primary production that exists across regional precipitation gradients contrasts with the low correlation between current-year precipitation and production at individual sites. Although arid ecosystems account for 40% of land surface and are home for 30% of human population, we still have a limited understanding of mechanisms controlling inter-annual variability of primary production. Lags in the response of ecosystems to changes in precipitation explain why current-year precipitation accounts for only a small fraction of the variability in production from year to year. Results showed that legacies occur through changes in the density of meristems (plant growing points). Previous dry or wet years differentially affected the components of asexual reproduction, which in grasses are tiller (shoot) density, stolon density, tiller growth, axillary bud density and percent viable axillary buds of black grama. Stolon and tiller density were the most sensitive parameters to changes in precipitation and were responsible for the observed lags in production. On the contrary, percent of active axillary buds was insensitive to changes in precipitation.

This work contributed to our understanding of temporal controls of ecosystem functioning in water-limited regions. Current-year production depends on current-year precipitation and previous-year precipitation. The effect of the latter is mediated by changes in stolon and tiller density. In addition, this work highlighted the differences between temporal and spatial controls on primary production.

Image caption: Rainout shelter used in the rainfall manipulation experiment at the Jornada LTER. Dr. Reichmann (pictured) and Dr. Sala studied lags in the response of productivity to changes in precipitation.
This paper can be found online here.

 

Variation in elemental stoichiometry and RNA:DNA in four phyla of benthic organisms from coral reefs.

Catherine Lovelock, Ruth Reef & John Pandolfi Reef-scape, Lizard Island lagoon. Photograph by Dr Ruth Reef.

The elemental composition of organisms, including carbon (C), nitrogen (N) and phosphorus (P) composition, is proposed to be linked to levels of RNA in organisms, which in turn influences rates of growth. In coral reefs, benthic corals and macroalgae (seaweeds) co-occur, competing for space on the reef. For these reasons we investigated elemental composition and RNA in reef corals and macroalgae at Lizard Island in the northern Great Barrier Reef lagoon. We surveyed species from four phyla and 53 genera, assessing the RNA:DNA ratio as an integrated measure of investment in nucleic acids to support growth. We tested a range of hypotheses aimed at increasing our knowledge of variation in elemental composition and RNA on coral reefs, including the role of phylogeny (genera, family, phyla) and of functional form. We found substantial support for links between elemental composition and RNA:DNA ratio in corals and algae. The RNA:DNA ratio was more closely correlated with N (and C:N ratio) than with P. Corals had higher concentrations of P and RNA:DNA ratios than macroalgae. Among the macrolagal lineages, consistent with hypotheses that predict higher C:P in lineages with low levels of complexity of their forms, C:P was higher in brown algae compared to red and green algal phyla. Genera of macroalgae with larger sizes tended to have higher N concentrations in their tissues than smaller forms. Analysis of phylogenetic sources of variation (family and genus) in elemental composition and RNA found that genus accounted for 15 – 47% of variation in both corals and macroalgae , but the largest source of variation (50-97%) was unexplained by our statistical model and thus most likely attributable to species, individual and environmental factors. Overall, variation in elemental composition of macroalgae was relatively low compared to that reported for terrestrial plants and was similar to that of corals. Our study shows that element ratios in marine macroalgae are different to terrestrial plants, which may underlie some of the differences between aquatic and terrestrial ecosystems, including more grazing but fewer specialist grazers in aquatic habitats. Additionally, our study indicates that theoretical models based on variation in RNA and elemental composition of corals and algae may be useful for predicting ecological interactions on coral reefs, although an enhanced understanding of uptake and storage of elements will be important for the development of models.

Image caption: Reef-scape, Lizard Island lagoon. Photograph by Dr Ruth Reef.
The article is available here.

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