The below summaries are provided by our authors to help put their research paper into context for the wider scientific community and the general public.
- Is parasitoid acceptance of different host species dynamic? Hopper et al
- Plasticity and genetics in un-invaded refuges: Possible consequences for native-exotic species co-existence Derry et al
- Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the Old and New World tropics Hodgkison et al
- Sex appeal is cheap for male threadfin rainbowfish Trappette et al
- Cafeterias are poor places to raise families Barea & Watson
- Can Plant-Microbe-Insect interactions enhance or inhibit the spread of invasive species? Bennett
- Three-way interactions between plants, microbes and insects: how do they adapt to each other? Biere and Tack
- Does herbivory influence litter decomposition of contrasted grasses in similar ways? Ibanez et al
- Ants, bees, and wasps team up with microbial symbionts for defense Kaltenpoth and Engl
- Coping with unpredictability in early life Homberger et al
- Seed harvesting is influenced by associational effects in mixed seed neighborhoods, not just by seed density Ostoja et al
- Climate warming and ectotherm body size – from individual physiology to community ecology Jan Ohlberger
- The use of leaf economics and size traits to classify woody and herbaceous vascular plants Pierce et al
- Pollinators, mates and Allee effects: the importance of self-pollination for fecundity in an invasive lily Rodger et al
- Removing nannies causes parents to spend more time with their kids… until a new nanny is found Bruintjes et al
- A novel framework to study colour signalling to multiple species Renoult et al
- Phosphorus content in detritus controls life history traits of a detritivore Danger et al
- Symbiotic fungi are the source of important chemicals in some plants Panaccione et al
- Plant pathogens impact insect communities Tack and Dicke
- Low resource availability may explain the limited growth of trees at the Arctic treeline McNown and Sullivan
- Why does wood in some trees get heavier as they grow and lighter in others? Strong radial variation in wood density follows a uniform pattern in two neotropical rainforests. Hietz et al
- How deep diving by elephant seal is rewarded by foraging success Naito et al
- Mechanisms of plant competition for nutrients, water and light Craine and Dybzinski
- Costs of dispersal and optimal offspring size in patchy habitats Burgess et al
- Better to be bigger or brighter as a juvenile poison frog? Flores et al
- Plant ecology’s guilty little secret: understanding the dynamics of plant competition. Trinder et al
- When food explains lower reproductive performance in a preferred habitat Hollander et al
- Risk of offspring predation drives nest success in a parental care-providing fish Zuckerman and Suski
- Maximum migration distances by sea turtles versus birds, fish and mammals Hays & Scott
- A simple idea to a complex problem: linking plants, animals and the environment. Frenette-Dussault et al
- Terminal investment in invertebrate males González-Tokman et al
- Plant-feeding by insect vectors can affect life cycle, population genetics and evolution of plant viruses Gutiérrez et al
- Better keep in shape: importance of being big and fat to use energy saving strategies in mouse lemurs Vuarin et al
- Even unlimited food can’t overcome the fitness costs of chronic immune challenge Stahlschmidt et al
- Plants give up rather than fight when facing strong competition Bonser
- Chemical espionage, manipulation and control in plant interactions with microbes and insects. Giron et al
- Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Pineda et al
- How are plants affected by simultaneous attack by insects and diseases? Hauser et al
- Aspects of plant volatile emission in response to single and dual infestations by herbivores and phytopathogens. Ponzio et al
- Keeping cool, fed and hydrated under environmental change Kearney et al
- A functional-comparative approach to facilitation and its context-dependence Butterfield and Callaway
- How plants compete with their neighbours Pierik et al
- Will adaptation rescue marine life from ocean acidification? Kelly and Hofmann
- Microbial mediation of plant competition and community structure. Hodge and Fitter
- Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Chevin et al
- Biophysical Effects on Plant Competition and Co-existence. Niklas and Hammond
- Difficulties in adapting to high temperatures. Hoffmann et al
Keith R. Hopper, Sean M. Prager, George E. Heimpel
The internal physiological state and previous experience of adult wasps whose larvae are parasitic on other insects can affect wasp egg-laying behavior among categories of host individuals (small versus large, previously parasitized or not) that differ in suitability for development and survival of wasp larvae. Female wasps with high egg loads and low life expectancy (i.e. time-limited) are more willing to accept hosts with low suitability for progeny development than females with low egg loads and high life expectancy (i.e. egg-limited). However, studies of egg-laying behavior in parasitic wasps have only considered high- versus low-suitability host individuals within the same host species. No one has tested whether internal physiological state and previous experience affects the egg-laying behavior in host species that differ in suitability. Here, we report the first results on whether egg-laying in host species that vary in suitability is dynamic in the same way as in host individuals that vary in suitability within species.
We studied two species of wasps that parasitize a narrow range of aphid species. We used two aphid species that both wasp species parasitize, but for which they have reciprocal egg-laying behavior, such that the aphid species with low suitability and thus low acceptance for egg-laying by one wasp species has high suitability and acceptance for egg-laying by the other wasp species. Contrary to predictions from theory and from studies within host species, we found that stressors (starvation and age) and experience did not affect egg-laying in low-suitability host species by these two wasp species. This result suggests that specificity is unlikely to change with internal or external conditions, at least for parasitic wasps with narrow host ranges. Three hypotheses might explain the stability of egg-laying behavior in these wasp species. First, if they frequently, but transiently, run out of eggs in the field because of the patchy distribution of highly suitable host species, they may undergo selection to lay eggs rarely in low-suitability host species because they will then not have eggs available when they encounter high-suitability host species. Second, they may achieve higher fitness from resorbing eggs rather than laying them in low-suitability host species because the nutrients from resorbed eggs can increase longevity and thus the likelihood of finding high-suitability host species. Third, they may have neural constraints on host recognition, i.e. limitations of nervous systems that restrict the rate of information processing. The first two hypotheses would apply equally well to generalist wasp species. However, if neural constraints restrict the ability of these specialist species to change their behavior under stress, we predict that generalist species will show greater dynamism in acceptance of low-suitability hosts. We are testing this prediction using parasitoid species with very broad host ranges.
Image caption: Adult wasp of a species (Aphelinus rhamni) whose larvae are endoparasites of certain aphid species.
Plasticity and genetics in un-invaded refuges: Possible consequences for native-exotic species co-existence
Alison M. Derry, Åsa M. Kestrup, and Andrew P. Hendry
One of the greatest contemporary threats to the biotic integrity of native aquatic communities is the invasion and rapid geographic spread of exotic species. Whereas much research is currently dedicated to factors controlling the establishment and impacts of exotic species in non-native habitats, little research has addressed how native species can mitigate the ecological impacts of invaders through evolution. In many cases exotic species can cause the extirpation of native species – but there are also circumstances that allow co-existence of native and exotic species within the same region. Our study integrates evolution into the domain of invasion biology to understand evolutionary conditions that can facilitate co-existence of native (Gammarus fasciatus) and exotic (Echinogammarus ischnus) amphipods (freshwater shrimps). Specifically, we consider how plasticity versus genetic/maternal effects in native amphipods that inhabit un-invaded refuges possibly contribute to native-exotic species co-existence in invaded habitats.
We anticipated high trait plasticity in the native amphipod because of high gene flow and high spatial and temporal environmental variation in our study system. Unexpectedly, we detected both plastic and genetic influences on the traits of native amphipods along natural gradients of calcium concentration in Lac St. Louis, QC, Canada. Plasticity was detected in only one trait, post-moult calcification, and three other traits (larval survival, time to first reproduction, and fecundity) were influenced by genetic variation or maternal effects that differed between calcium-rich and calcium-poor habitats.
Both plasticity and genetic/maternal effects likely enhance the ability of native amphipods to inhabit a broad spectrum of calcium concentrations. While the most successful invaders tend to be generalists that can displace specialist natives in many cases, our findings suggest that the converse can also be true, and highlight the conservation value of calcium-poor refuges that exotic amphipods cannot tolerate. Adaptive phenotypic variation in native amphipods potentially enhances the effect of calcium-poor refuges in providing surplus native individuals that can disperse into invaded habitats where they coexist with exotic amphipods. Future work will address the net effect of multiple influences from plasticity and genetic/maternal effects on overall fitness of native amphipods dispersing from calcium-poor, refuge habitats into calcium-rich, invaded habitats.
Image caption: Lac St. Louis, QC, Canada (facing west from Montreal), showing distinct calcium-rich (left) and calcium-poor (right) water masses. The native amphipod persists across this calcium gradient, but the exotic amphipod is restricted to calcium-rich habitats. Photo credit: St. Lawrence Centre, Environment Canada.
Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the Old and New World tropics
Robert Hodgkison, Manfred Ayasse, Christopher Häberlein, Stefan Schulz, Akbar Zubaid, Wan Aida Wan Mustapha, Thomas H. Kunz and Elisabeth K. V. Kalko
Bats are important seed dispersers for many tropical plants. Fruit consumption by bats is believed to have evolved at least twice: once in the Old World tropics (in Africa, Asia, and the Pacific) within the flying fox family (Pteropodidae), and once in the New World tropics (Central and South America) within the leaf-nosed bat family (Phyllostomidae). Bats from both families have a keen sense of smell, which they use to locate fruits. However, it is currently unknown whether bats from both families share a preference for the same types of scent.
To explore this idea, we conducted fieldwork in Malaysia and Panama to collect the natural fruit scents of wild figs. We also performed behavioural experiments on bats to test whether natural fig fruit scents from both regions would induce the bats to feed. The bat species selected for these experiments were the short-nosed fruit bat (Cynopterus brachyotis) in Malaysia, and the Jamaican fruit bat (Artibeus jamaicensis) in Panama.
We discovered that figs, from both Malaysia and Panama, had chemically similar fruit scents--dominated by a group of chemicals known as monoterpenes. Interestingly, these monoterpenes were completely absent from similar, closely-related fig species consumed by birds.
Closely-related fig species, consumed by bats, produced chemically similar fruit scents. However, one group of figs from Malaysia (from the sub-genus Sycomorus) proved to be an exception. The fruit scents of these figs were highly variable, sometimes completely lacking monoterpenes, which suggests that their interactions with bats are likely to be less specialized. In other words, in addition to bats, these Old World figs are likely to be consumed by a broad range of other seed-dispersing animals.
Consistent with this view, Jamaican fruit bats, from Panama, clearly preferred fruit scents with monoterpenes, and were attracted to similar fruit scents from both Panama and Malaysia. Short-nosed fruit bats from Malaysia, by contrast, were only attracted to fruit scents from Malaysia, and rejected chemically-similar fruit scents from Panama. Short-nosed fruit bats also consume Sycomorus figs, which may lack monoterpenes, so in this species, no obvious fruit scent preference could be discerned.
Image Caption: A short-nosed fruit bat (Cynopterus brachyotis) eating a fig (Ficus hispida). Photo by Rob Hodgkison.
Andrew Trappett, Catriona H. Condon, Craig White, Phil Matthews & Robbie S. Wilson
A basic assumption of evolutionary ecology is that sexiness is costly – otherwise, why wouldn’t everyone be sexy? It’s believed that only the best individuals are able to bear the costs associated with excessive attractiveness; that developing and maintaining an outrageously elongated tail, or heavy horns, or conspicuously-bright scales takes a lot of energy or increases the individual’s risk of being spotted and captured by a predator.
A male who can thrive in spite of his sexy features? Now that’s attractive.
We tested this assumption by measuring the costs and benefits associated with the long, flamboyant fins of male threadfin rainbowfish. Found in streams and lakes across the top-end of Australia, threadfin males develop extensive, trailing fin streamers, presumably at great cost to their swimming abilities. Swimming is an energetically expensive activity, and changes to a fish’s hydrodynamic profile – for example, via a greatly-elongated fin – should increase the energy needed to swim and decrease its overall swimming performance. To see if this was the case, we measured the metabolic rates and sprint swimming speeds of male fish with varying natural fin lengths, and then re-measured males after experimentally shortening their fins.
We found, as expected, that female threadfins preferred males with longer ornaments; but we were surprised to find no evidence that longer fins were hydrodynamically costly to males. Males swam just as fast after their fins were shortened as before, and fin size didn’t affect metabolic rates during swimming.
Ultimately, our results didn’t support the idea that sexiness is a burden. Is this because it isn’t? Not exactly – a threadfin’s ornaments didn’t affect its metabolic rate or swimming speeds, but that doesn’t mean these traits aren’t costly; it could merely mean that we didn’t measure the right thing. Our next step in this research will involve looking at how ornament length relates to a male’s ability to survive in more-natural conditions, where escaping predation depends on more than just swimming fast.
Threadfin rainbowfish (Iriatherina werneri). Photo provided by authors.
Laurence P. Barea and David M. Watson
Mistletoes are parasitic plants that grow in forest canopies throughout the world, reliant on birds to spread their seeds from one tree to another. In many regions, mistletoes are among the few plants providing fleshy fruits, and they represent important food resources for many different species. While interactions between mistletoes and fruit-eating birds have been well studied, other aspects of these plants are less understood. With their succulent leaves and rigid stems, mistletoes form discrete clumps that are highly favoured as nest sites by many birds and mammals. These two sets of resources—nutritious fruits and secure nesting sites—have been the focus of numerous ecological studies but, so far, this work has been conducted in parallel. We focused on the painted honeyeater, a poorly-known Australian songbird that uses one genus of mistletoe (Amyema) as a nest site and principal food source, the first study to consider both resources simultaneously. We conducted this work over two breeding seasons in a semi-arid woodland in southern Australia, near the town of Griffith.
Most painted honeyeater nests were in mistletoe, or in areas of high mistletoe abundance, consistent with our expectation that they nest close to their favoured food source. But, when we looked at how successful the nests were (in terms of how many chicks were reared) we found something we weren’t expecting: nests in mistletoe were far less successful than nests placed in trees, and this difference was due entirely to increased levels of predation.
Since painted honeyeaters are reliant on mistletoe fruit as their main food source (even feeding the berries to their chicks), the nesting period coincides directly with the time of greatest fruit abundance. Many other birds, including several honeyeaters known to eat chicks and eggs, also live in this woodland, regularly visiting fruiting mistletoe plants. So, rather than gaining any advantages by breeding close to their food source, those birds nesting in mistletoe ended up losing most of their chicks to opportunistic visitors.
Image caption: A male painted honeyeater Grantiella picta, singing from a perch beneath a grey mistletoe Amyema quandang. (Photograph by Chris Tzaros, used with permission).
Special Feature: Plant-Microbe-Insect Interactions
Alison E. Bennett
Invasive species are species newly introduced to an environment that cause changes to ecosystems and economic losses. Naturally such species interact with resident natives, and with other introductions, in novel and unexpected ways. The interactions that arise from the introduction of new plant, insect, and microbe species can be described as the new field of Plant-Microbe-Insect (PMI) Interactions.
While we might predict that novel PMI interactions are likely to be simple due to their relatively short period of interaction, I show that these interactions are often much more complex than expected. Instead, there are a surprising number of non-additive synergistic interactions that occur with invasive species. Synergistic interactions are those that cannot be predicted simply by adding together their simpler component pairwise interactions (e.g. plant-insect and plant-microbe).
I document a number of instances where invasive species are promoted by novel PMI interactions. For example, invasive plants have been shown to be promoted by microbial endophytes that live within host plant tissues and reduce feeding by insect herbivores, invasive insects can increase the spread of both native and invasive microbial pathogens, and microbes that live symbiotically within insects can promote both the invasion of their insect hosts and the spread of other microbes. There are cases where PMI interactions limit invasive species, but these predominantly arise from deliberate attempts at biocontrol, for example a synergistic effect of an insect herbivore and a pathogen on an invasive plant. But there are still relatively few such examples, suggesting a wide area of research still to be addressed.
Future research on novel PMI interactions should focus on predicting those interactions that promote invasive species, and identifying existing PMI interactions that could be manipulated to hinder the spread of invasive plant, microbe and insect species.
Image caption: The invasion of Bodega Bay Marine Reserve by the invasive grass Holcus lanatus. H. lanatus alters soil microbial communities and we suspect insect communities.
Special Feature: Plant-Microbe-Insect Interactions
Arjen Biere and Ayco J.M. Tack
In nature, plants often interact with both insects and microbes. For instance, many plants interact with insect pollinators that are beneficial for the plant, but also with plant eating (herbivorous) insect that generally have detrimental effects on the plant. Similarly, plants interact with microbes (viruses, bacteria, fungi, etc.) that can be beneficial for plants, like root-associated bacteria and fungi that promote plant growth, as well as microbes that are detrimental to the plant, like plant pathogens that cause disease. Interestingly, infection of plants by microbes often leads to changes in plant traits (for instance leaf concentrations of minerals or toxins) that subsequently affect their suitability as a host plant for herbivorous insects. Similarly, insect herbivores can alter the quality of their host plants for the microbes that are associated with these plants. This leads to important three-way interactions between plants, microbes and insects.
Some studies have documented that individuals of particular insect or microbe species perform better on plants (of a particular host plant species) that originate from the same locality as the insects or microbes, than on plant individuals that originate from another locality. This is known as local adaptation. In this specific case, the insect or microbe is said to be locally adapted to the host plant, that is it can better exploit local host plants than non-local host plants. This is assumed to result from natural selection in the local environment.
Local adaptation has so far mainly been studied in interactions between two species, for instance between insects and their food plants. However, since we now know that the characteristics of these host plants (their phenotype) can be strongly affected by interactions with microbes or other “hidden players”, the question arises whether herbivores do not “just” adapt to their host plants, but in fact adapt to the specific plant phenotypes that result from their interactions with other players like their local microbes. Our review summarizes the emerging evidence that this is indeed the case. Therefore, it is very important to study local adaptation between two species in the proper ecological context, incorporating the effects of such “hidden players”.
Image caption: A caterpillar of the moth Hadena bicruris is forced to eat flowers instead of fruits (its primary food source) on its host plant (White Campion, Silene latifolia) because a fungal plant pathogen (the anther smut Microbotryum violaceum) has prevented the plant from producing fruits. This is an example of a three-way interaction between plants, microbes, and arthropods. The moth has evolved an adaptive response: she avoids laying eggs on infected plants. (Photo credit: Arjen Biere)
Sébastien Ibanez, Lionel Bernard, Sylvain Coq, Marco Moretti, Sandra Lavorel & Christiane Gallet
When herbivores eat leaves, plants may alter their chemical composition. For example, herbivory can induce the production of defensive compounds such as phenolics. If these changes are still present after leaf senescence, they can affect litter decomposition. This phenomenon has rarely been studied for grasses, which contain fewer defensive compounds than trees or broad-leaved herbs. Grasses include species having either permanent or induced defences, so we expect that depending on the grass strategy against herbivores, herbivory would differentially alter litter decomposition.
We conducted an experiment in which mountain fescue, Festuca paniculata (permanent defences) and cocksfoot, Dactylis glomerata (induced defences) were consumed by grasshoppers. We studied the speed of litter decomposition and measured the chemical composition of fresh, senescent and decomposed leaves, focusing on their carbon:nitrogen ratio and on phenolics.
Grasshoppers did not modify the carbon:nitrogen ratio of D. glomerata leaves, but they induced the accumulation of phenolics. However, most phenolics were lost during senescence, so that grasshoppers did not influence the litter decomposition rate.
Grasshoppers slightly increased the carbon:nitrogen ratio of F. paniculata, but the litter decomposition rate did not depend on this chemical ratio, contrary to previous findings. Grasshoppers did not induce the accumulation of phenolics in fresh leaves, but they increased the rate at which they disappeared during senescence. Interestingly, this led to a decreased litter decomposition rate, probably because the phenolics of this fescue are substrates for microbes and enhance decomposition.
We conclude that depending on the characteristics of grasses, in particular the way they respond to herbivory, herbivory can have contrasted effects on their litter decomposition, which might lead to complex outcomes at the ecosystem level.
Male grasshopper (Chorthippus scalaris). Photo credited to Sébastien Ibanez.
Special Feature: Defensive Symbiosis
Martin Kaltenpoth and Tobias Engl
Insects encounter a multitude of natural enemies, ranging from vertebrate and invertebrate predators to parasites and microbial pathogens. Many species in the insect order Hymenoptera (the ants, bees, and wasps) are especially vulnerable to pathogen infection, because they – like humans – live in large societies that allow detrimental fungi, bacteria and viruses to spread, and/or because they develop in underground nests, surrounded by a plethora of potentially dangerous soil microbes. To counteract these threats, insects have evolved mechanical, chemical and behavioral defenses as well as a complex immune system. In addition to the host‘s own defenses, however, some Hymenoptera team up with protective microbial helpers.
As more and more insect-bacteria symbioses are being discovered, it becomes increasingly clear that such defensive alliances constitute an integral part of insect ecology. In leaf-cutter ants and beewolf wasps, symbiotic bacteria produce mixtures of antibiotics that protect the food resources or the developing offspring against pathogenic fungi. Bumblebees cultivate intestinal microbes that fend off a parasitic protozoan, a close relative to the causative agent of human sleeping sickness. And parasitic wasps that develop in living caterpillars team up with symbiotic viruses to protect themselves against the caterpillar’s immune response. Thus, protective symbioses can be important in a variety of different contexts, and the study of such interactions not only yields insights into an as yet little-understood aspect of insect biology, but may also provide new ideas for sustainable control of increasingly resistant human pathogens. After all, with the help of their symbionts, some insects have successfully combated pathogenic microbes for millions of years.
Image caption: Female beewolf wasp (Philanthus coronatus) with prey. Beewolves team up with symbiotic bacteria that produce antibiotics and thereby protect the wasp offspring against detrimental microbes. Photo: M. Kaltenpoth.
Benjamin Homberger, Susanne Jenni-Eiermann, Alexandre Roulin and Lukas Jenni
Understanding how organisms cope with their environment and why they show different survival strategies is crucial in a changing world. An organism’s characteristics are shaped by the interplay of genes and environmental conditions which ultimately affect physiology, behaviour and fitness. Early developmental conditions (e.g. nutritional supply in prenatal or early life) can profoundly affect an individual’s traits later in life. However, adverse prenatal or early life conditions do not necessarily entail detrimental consequences but can act as developmental cues that allow an organism to adapt to these specific environmental conditions. For example, a mother can react to environmental perturbations (e.g. infections or food shortage) during gestation or egg-laying by transferring messenger chemicals (hormones, maternal antibodies) to her embryos or eggs. Her offspring might then profit in terms of enhanced immunity or decreased energetic demands. But physiological systems such as the immune system or the physiological stress response not only provide essential functions but are also costly. A cost of many physiological systems is the production of free radicals, which can damage cells. Thus, an organism’s physiology has to be well orchestrated and carefully adjusted to the environment it functions in.
We investigated in grey partridges from wild and domesticated origin how they physiologically cope with pre- and postnatal unpredictable food supply by measuring indices of stress physiology, immunity, energy production and resistance to free radical attack. Wild birds had a strong stress response and immune response and had a good resistance to free radical attack which could benefit them in the wild. However, their strong physiological stress response was ill-fitted to the captive environment. Because of their strong reaction to the everyday stress of an unpredictable captive environment, their resistance to free radicals was markedly reduced. On the other hand, wild birds reacted to prenatal unpredictable food supply by lowering their stress response and thereby reducing the production of free radicals. Contrarily, domesticated birds showed relatively lower stress response, immune response and resistance to free radicals. Nor did they adjust their offspring’s physiology to prenatal conditions.
In all birds we found that postnatal food unpredictability caused a lasting boost in the bird’s immunity, improving their ability to fight infections. In essence, our study highlights important differences and coping strategies between wild and domesticated birds and it sheds light on the complex interplay of physiological systems which can profoundly affect an organism’s life-history.
Grey partridge chick around 1 week old. Early life conditions can profoundly affect an individual’s traits later in life. Photograph by Markus Jenny.
Seed harvesting is influenced by associational effects in mixed seed neighborhoods, not just by seed density
Steven M. Ostoja, Eugene W. Schupp, Susan Durham and Rob Klinger
Seed eating animals, or granivores, are expected to harvest more seeds where more seeds are found. In nature, many different seed species generally occur mixed together, so granivores have to make harvesting decisions in the face of complex mixtures of seed species in a patch rather than seeds of only a single species. The species makeup of these local seed mixtures can affect these harvesting decisions. Consequently, a seed’s likelihood of being harvested is not only influenced by its own characteristics, but also by the characteristics of neighbouring seeds. These interactions among co-occurring seed species that affect harvesting by granivores result in associational effects; that is, the association of one species with another determines how much of each is harvested. Two types of associational effects are possible. Associational resistance occurs when a granivore’s harvesting of one seed species is decreased by the presence of another seed species. Alternatively, associational susceptibility occurs when the presence of one seed species increases the harvest of a second seed species. Granivory is a critical plant-animal interaction in desert ecosystems in western North America; ecosystems threatened by non-native annual grass invasion that may disrupt seed-seed consumer interactions. In this context, we tested first whether the amount of seed available affected seed harvesting. Second, and more important, we tested for associational effects in mixtures of seeds of native perennial grasses and seeds of the invasive annual cheatgrass. The proportion of native seed harvested increased with the amount of native seed available, as expected. In addition, native seeds were harvested less when cheatgrass seeds where present, indicating associational resistance, although exact patterns differed among native species. Conversely, more cheatgrass seeds were harvested when present with native seeds than when alone, indicating associational susceptibility. Our results suggest that seed mixtures, the relative densities of seeds in the mixture and seed species all influence rodent granivore foraging behaviour.
The implications of these results are two-fold. Invasion by non-native species affects the seed foraging behaviour of the species in our ecosystem. As such, considering how differential seed harvest translates to plant population and community dynamics in the face of invasion is critical. Second, in ecological restoration seeds are often applied to disturbances in large quantities in mixtures. If we understand associational effects sufficiently to develop mixtures with particular species in particular quantities that improve the chances of more desirable species establishing, the success of restoration efforts likely can be improved.
Image caption: Mixed seed species
Climate warming can have profound effects on animal species. The most commonly observed responses to climate warming are shifts in species’ geographic distribution and the timing of biological events. Recently, declines in average body size have been reported across a range of species and suggested to represent a universal response to increasing temperatures. Such shifts can have severe consequences for the structure and functioning of ecosystem and thus the services they provide for humans. However, our knowledge about the causes of declining body sizes and how these vary between species and environments is limited.
In this study, I summarize evidence for the effects of rising temperatures on the mean body size and the distribution of sizes within populations. I show how different mechanisms determine organism responses to climate warming in complex ways and at different levels of organization, from individuals to entire food webs. These mechanisms include physiological effects on individual growth and development, changes in ecological interactions such as size-dependent survival or dispersal, and shifts in the species composition of a food web.
While we generally understand how single organisms respond to temperature changes under laboratory conditions, in nature the actual response of a population will depend on complex interactions with potential competitors, predators and prey. Considering the broader ecological context is therefore necessary when trying to understand the underlying causes of declines in mean organism body sizes. A better functional understanding will help to improve our predictions about future changes and the management of ecosystems in the face of a warming climate.
Image caption: European grayling (Thymallus thymallus). Photo taken by Jan Ohlberger.
Simon Pierce, Guido Brusa, Ilda Vagge and Bruno E. L. Cerabolini
A vast number of plant species carpet the terrestrial landscape; diversity that is hard to come to terms with by investigating the peculiarities of each species one at a time. However, where plants grow in similar circumstances similar lifestyles and physiologies are apparent. By measuring the traits associated with these lifestyles the bewildering diversity of species can be reduced into a manageably small range of survival strategies that can help us to understand how diversity develops, how communities of species form and how species affect the working of ecosystems. The study published in this edition of Functional Ecology is based on the variability of traits involved in plant competition and resource use, and combines these trait values into a practical tool allowing the quantification of the overall survival strategy. Whilst this has been possible in one form or another for some time, recent advances in our understanding of how traits vary worldwide indicate that a small number of leaf traits are particularly important and representative of the overall strategy, and are shared by a broad swathe of plant life including ferns, gymnosperms and both herbaceous and woody flowering plants. Fortunately these traits are relatively straightforward to measure, and the new method will allow ecologists to rapidly compare the survival strategies of huge numbers of plants growing in their natural environment. In this way, different species within a community can be compared, different communities can be characterized, and even the differences within populations of single species can be measured. The new method, known as CSR classification after the theory of Competitor, Stress-tolerator and Ruderal strategies developed by British ecologist Philip Grime and co-workers, is based on traits measured for wild herbaceous and woody plants from a broad range of habitats spanning the high alpine zone of the Italian Alps (see photo) to the continental climate of Lombardy’s lowlands.
Image caption: Bruno Cerabolini (University of Insubria) and co-workers identify and collect plant material near the Stelvio pass on the border between Italy and Switzerland, as part of a study of the life-history traits of hundreds of species from a range of habitats. This led, in the current issue, to the production of a novel method for quantifying and comparing plant survival strategies (photo: Simon Pierce).
Pollinators, mates and Allee effects: the importance of self-pollination for fecundity in an invasive lily
James G. Rodger, Mark van Kleunen and Steven D. Johnson
Biologists lack a good understanding of what causes some species to invade natural habitats, after people introduce them to new environments, while others do not spread successfully. Initially, only a few individuals may be present and after dispersal, single individuals are isolated from the original population. Clearly, the chances that invasion takes place are greater if plants in these small populations can reproduce successfully. Small isolated plant populations attract fewer pollinators. Furthermore, pollinators that visit single isolated plants may not be carrying pollen from other plants of the same species. Recent studies have shown that plant species in which individuals are capable of being fertilised by their own pollen are more likely to be invasive than those that need pollen from another individual (the case in around 50% of flowering plants). However, there has not been any direct evidence that this is because self-fertilisation mitigates effects of low population size or isolation on reproduction. We tested this hypothesis in Lilium formosanum, a Taiwanese lily species invasive in South Africa. Although a giant hawkmoth pollinates their flowers, plants are also capable of self fertilisation in the absence of pollinator visits.
We prevented self-fertilisation in Lilium formosanum by emasculating flowers – removing their male pollen-producing parts – in 66 ‘naturally occurring’ invasive populations ranging from 1 to 6000 individuals over three years. Emasculation reduced seed production by two thirds. This shows that Lilium formosanum depended on self-fertilisation for at least this fraction of its seed production, due to infrequent pollination by hawkmoths. However, this was not related to population size. We also artificially isolated emasculated plants 3-702m from two ‘naturally occurring’ populations, and put either a second emasculated plant or an intact plant – one that still had its male parts and could supply pollen – next to each of these emasculated plants. Isolation increased dependence on self-pollination for seed production, but only in the absence of a pollen supply. This shows that moth pollinators visited isolated plants as frequently as non-isolated plants, but were less likely to be carrying the right kind of pollen when they visited isolated plants. Observations of hawkmoth body scales and pollen, deposited on emasculated flowers, supported this conclusion. This is the first study to show that self-fertilisation may facilitate invasion by increasing reproduction especially in isolated plants, and uses new methods to separate effects of pollinator visitation from pollen availability.Image caption:Agrius convolvuli pollinating Lilium formosanum. Photo Steve Johnson.
Rick Bruintjes, Zina Heg-Bachar and Dik Heg
In social group-living species that help each other (for example non-dominant group members in meerkats) “nannies” may help raising the kids. Parents can benefit from this help by (1) the extra attention that their kids get or (2) they can reduce their own time raising the children without having to worry that the kids do not get enough attention. In the social fish Julidochromis ornatus, one large male helper (the nanny) spends almost all of his time close to the breeding shelter, whereas the dominant pair (the parents) is only around half of their time.
We removed this large helper for 30 days – which is one breeding cycle in these fish – and studied the investment strategies of the dominant pair and whether the survival of their brood was affected, while checking for immigration of new helpers. On day one and day seven following removal, we tested whether dominants made up for the absence of the helpers and, if they did, which parental behaviours were affected.
One day following the removal, the dominant pair spent more time in their territory, visited the breeding shelter more and defended their territory more against other fish in comparison to the pre-removal phase and the control groups where we did not remove the large helper. Seven days after removal, no differences between the control and removal group were seen. However, in some removal groups a new large helper became part of the group. Our data show that the dominant pair only spent less effort in their breeding shelter visits, defence and time spent in the territory when a new large helper was present in their territory. Finally, survival of the juvenile group members was not affected by removal of the large helper.
Our experiments show that large helpers in these fish allow the dominant male and female to reduce their personal contribution to their offspring and territory. Moreover, we highlight the importance of immigration of new large helpers to relieve dominants from carrying out parental behaviours in cooperative breeding systems.
Image caption: A picture of J. ornatus . Source: http://www.riftlakes.com/cichlids/julidochromis_ornatus_e.html
Julien P. Renoult, Alexandre Courtiol and H. Martin Schaefer
Over the last two decades, ecologists have used physiological models to understand how the ecology and evolution of animal communication are influenced by animals’ sensory perception of the world. The perception of signals has been mostly modelled in communication systems with a single perceiving species. In natural conditions, however, communication frequently involves several species e.g., if a flower is pollinated by bees and butterflies. Recently, it has been recognized that even communication systems that were previously thought to be highly specific were best understood when studied in a wider ecological context. In mating systems, for example, predators try to benefit from the decreased awareness of displaying males. In this case, females and predators jointly select male sexual signals. A thorough understanding of animal ecology and evolution thus needs to compare how the multiple species contributing to a communication system perceive a given signal. Unfortunately, current models of sensory perception do not allow such comparisons.
Here, we introduce a method to compare colour vision between species even if these differ in their sensory perception. We present the mathematical underpinnings of the method and apply it to study colour signalling in birds. In the above example of sexual communication, one response to the antagonism between selection by females and by predators is the evolution of private communication channels, i.e. colour signals that are conspicuous to the former but not to the latter. We revisit the classical paradigm that songbirds have evolved private communication channels, exploiting the difference in colour vision they have with their main predators, birds of prey. We show that yellow, not ultraviolet colours as previously thought, maximise the difference in conspicuousness to songbirds and to birds of prey. However, we found no evidence of private visual communication in songbirds, which may be explained by the similarity in colour vision of songbirds and birds of prey. Our method can be easily applied to other systems of visual communication and is theoretically transferable to other sensory modalities. We expect it will significantly improve our understanding of communication by extending the focus from signaller-perceiver pairs to ecologically more realistic conditions of communication among multiple species.
Image caption: Communication systems often involve multiple perceivers. For example, most flowering plants are pollinated by several insect species. Floral colouration should thus be adapted to communicate through different visual systems. Source: Creative Commons.
Michael Danger, Julio Arce Funck, Simon Devin, Julie Heberle and Vincent Felten
Since most living plant material is not consumed by herbivores, many ecosystems rely on plant detritus (leaf litter, dead wood…) as the main source of nutrients and energy. Detritus is then consumed by detritivores (mainly invertebrates), these organisms representing the essential basis of food chains. Forested headwater streams are typical detritus-based ecosystems where the detritivore communities are often dominated by insect larvae and small crustaceans. In Western Europe, Gammarus fossarum is one of the most common crustacean detritivores found in small forested streams, where it represents an important component of fish diet.
A central question in ecology concerns the drivers of biological production and, in particular, which factors limit organisms’ growth and development. For decades, food quantity available for consumers has been considered as the most important parameter controlling organisms’ growth. More recently, it has been proposed that food content of some essential chemical elements (food quality) could be directly involved in the control of organisms’ growth. Among these chemical elements, phosphorus is a key component of many biological molecules (such as DNA or RNA) and it is now recognized that this element can potentially limit the growth and reproduction of many herbivore species. Despite the importance of detritus-based ecosystems on Earth, extremely few data are available on the role of detritus chemical element content for detritivore species.
In this study, we manipulated the phosphorus content of two leaf litter types resulting in a large gradient of detritus chemical quality. The detritus was then used to feed individual G. fossarum during a 5-week experiment under controlled conditions. Size growth, mass growth and molt number were determined throughout the experiment. Our results showed for the first time that phosphorus enrichment of detritus led to faster growth of detritivores, whatever the leaf litter type considered. For both leaf litter types, survival rate of G. fossarum was positively correlated with detritus phosphorus content. This study sheds new light on the importance of phosphorus content of detritus for detritivorous organisms, and paves the way for further studies aimed at understanding the physiology of detritivores and the functioning of detritus-based ecosystems.
Image caption: Precopulatory mate guarding in Gammarus fossarum (Crustacea Amphipoda; male above) and details of the primary flagellum segments counted to assess gammarids molts.
Special Feature: Defensive Symbiosis
Daniel G. Panaccione, Wesley T. Beaulieu and Daniel Cook
Many plants live in mutually beneficial partnerships (symbioses) with fungi that inhabit internal tissues of the plant. These beneficial fungi, known as endophytes, often produce chemicals that protect the plant from insects and grazing animals. The host plant, in turn, provides nutrients and a protected place in which the fungus can live. In some cases of symbioses, the fungus never leaves its host plant; it grows from generation to generation through seeds of the plant. In other cases, fungi may be spread infectiously from one plant to another. In this article we review and summarize the published scientific work on symbiotic fungi that produce noteworthy chemicals in plants. Plants containing these fungi have been known to naturalists or agriculturalists for centuries as being poisonous or as sources of biologically active chemicals; however, research has shown that in the cases that we summarize, symbiotic fungi (as opposed to the plants themselves) are the sources of the important chemicals. Published work indicates that plants and fungi from different families participate in these symbiotic partnerships and that partnerships between plants of different families and their symbiotic fungi arose independently on different occasions. The data also indicate that the ability of the fungus-produced chemicals to protect plants from insects may have been an important factor in the establishment of symbioses between endophytic fungi and plants. We propose that scientists need to further study the possibility that other important chemicals associated with plants may be produced by previously undetected symbiotic fungi in those plants.
Image caption: Leaves of Ipomoea asarifolia lacking (top) or containing (bottom) symbiotic fungus Periglandula ipomoeae.
Special Feature: Plant-Microbe-Insect Interactions
Ayco J.M. Tack & Marcel Dicke
Plants are often attacked by a diverse community of insect herbivores and plant pathogens. In both agricultural fields and natural communities, these insect and pathogen species commonly co-occur on the same plant individual (see figure). Hence, one would expect direct and indirect interactions to occur among herbivores, among pathogens, and also between herbivores and pathogens. However, while we have known for decades that pathogens interact with pathogens, and herbivores with herbivores, the interactions among pathogens and herbivores have received relatively little attention.
Such neglect of the role of pathogen-herbivore interactions may be due to two historic reasons. First, the individual development of the disciplines of plant pathology and entomology has, despite several attempts to bridge both fields, so far resulted in relatively limited cross-disciplinary experimentation. Second, one of the classic tenets of competition theory states that competition is strongest among closely related species. While the latter view has received only weak support in a recent quantitative review on plant-feeding insect communities, it may well have discouraged early attempts to investigate pathogen-insect interactions.
In this perspective, we explored the literature to exemplify how pathogens may impact herbivore communities. Our results demonstrate that pathogens can both positively and negatively affect herbivore performance, preference and population dynamics, depending on the identity of the pathogen and herbivore. Such species-specific responses result in changes in the composition of the insect community in the presence of a plant pathogen: if one herbivore thrives and another not, this will affect their relative abundances. Fascinatingly, the pathogen may also affect the attack rate of the herbivore by its natural enemies, like parasitoids and predators.
Our synthesis of the literature illustrates that the largely unexplored interactions between pathogens and herbivores are common and diverse. Moreover, the impact of pathogens on herbivores can be as strong, or even stronger than, interactions among herbivores themselves. For these reasons, we argue that unravelling the mechanisms behind pathogen-insect interactions is crucial for our fundamental understanding of terrestrial plant-based communities. Equally important, insights into pathogen-insect interactions may inform applied scientists devising integrated pest management strategies against both plant pathogens and insect herbivores.
Image caption: Plants are often simultaneously attacked by pathogens and herbivores. The photo shows a black mustard leaf (Brassica nigra) with damage by a bacterial pathogen and feeding damage by cabbage white caterpillars (Pieris brassicae). Photo courtesy Hans Smid, www.bugsinthepicture.com.
Robert W. McNown and Patrick F. Sullivan
The boreal forest covers a vast land area and its limits are moving further north in many locations. The amount of land surface that is covered by forest versus tundra is important to regional and global climates. In order to predict where and under what circumstances we might expect changes in treeline, we need to improve our understanding of the factors limiting the performance of treeline trees. An improved understanding of the controls on the treeline will then enable more informed predictions of how treelines might respond to future climates.
It has long been thought that growth of treeline trees is directly limited by cold temperatures during the growing season. Researchers hypothesized that treeline trees have all the resources necessary to support growth (carbon taken up through photosynthesis and nutrients from the soil), but that cold temperatures limit cell division and growth. However, detailed studies of the performance of trees at the Arctic treeline are rare and this hypothesis remains largely untested.
To improve our understanding of the relationships between temperature and performance of white spruce near the Arctic treeline, we made measurements of photosynthesis, needle nutrition and soil nutrient availability over two years in three contrasting habitats of northwest Alaska: riverside terrace, hillslope forest and treeline. The sites had similar aboveground climates, but very different soil conditions. Soils were warm and dry on the terrace, cool and moist in the forest and cold and seasonally wet at the treeline. Photosynthesis, needle nitrogen (N) concentration, and soil N availability declined from the terrace to the forest to the treeline.
Contrary to the prevailing hypothesis, our results suggest that low resource availability may explain the limited growth of trees at the Arctic treeline. We hypothesize that low soil N availability reflects limited microbial activity in the cold treeline soils. Soils are particularly cold in winter, as the treeline maintains a shallow snowpack that poorly insulates the soil from cold air temperatures. Our results highlight the potential for an indirect effect of temperature on the growth of trees at the Arctic treeline and suggest that treeline responses to changes in climate may be more complex than previously thought.
Image caption: Treeline Study Site in Northwest Alaska
Why does wood in some trees get heavier as they grow and lighter in others? Strong radial variation in wood density follows a uniform pattern in two neotropical rainforests.
Peter Hietz, Renato Valencia and S. Joseph Wright
Wood keeps a tree upright, transports water from the roots to the leaves, stores water and carbohydrates and needs to be defended against pathogens. As trees grow from small saplings to tall individuals, the wood function and structure best suited for that function may change, with the changing needs during a tree's lifetime reflected in a gradient in the wood from the stem center to the bark.
Heavier (denser) wood is generally stronger, and wood density is known to be related to a tree's resistance to drought and pathogens, and to several other functions, but denser wood is also more costly to produce. Foresters are well-aware that wood density changes from the center to the bark in some trees and not in others, but why density increases, decreases or remains constant remains unclear.
We collected wood cores with the increment borers foresters use, split these into 5-cm segments from the innermost to the outermost part, and measured wood density of each segment, so that radial changes in density were obtained. This was done for hundreds of species in two rainforests in Panama and Ecuador. In these well-studied forests, tens of thousands of trees are monitored, so that characteristics such as size, growth and mortality of the species are known, which are important to understand the function of other traits such as wood density.
In many trees wood density increases as they grow, in a few it decreases. While generally trees with light wood tended to grow faster and die faster, radial changes in density were not directly related to demography. However, we found a very clear pattern showing that when trees start with light wood it tends to get heavier later, while in trees with heavy inner wood, the density remains constant or even decreases.
Wood density is needed to calculate the biomass and carbon stored in a tree, and when density within a tree changes in ways that we do not understand, this may produce errors in biomass estimates. Finding a fairly uniform pattern in radial density variation may thus help to reduce these errors.
Image caption: Getting to the heart of this rainforest tree to understand radial variation in wood density is hard work. Photo credid: Peter Hietz.
Yasuhiko Naito, Daniel P. Costa, Taiki Adachi, Patrick W. Robinson, Melinda Fowler and Akinori Takahashi
Many mammals, seabirds and even sea turtles dive deep in the ocean, well below the well-lit zone of about 150-200m, and some whales and seals dive into true darkness at extreme depths of over 1000m. The northern elephant seal is one such extreme deep diver. While dive time is extremely limited by O2 store, they dive deep (400–700 m, and up to 1754 m) to forage for extended periods (~22 min) and repeat such dives without taking rests at the surface. While seals dive deep continuously, they also migrate several thousand km to the northeast Pacific Ocean from California. How the seals forage successfully in deep water by continuous deep diving is not understood. A key to understanding their behavior is to observe their feeding, and to try to do this we developed a jaw motion recorder, using an accelerometer, that allowed us to measure feeding events and dive depths for several months. We used this technique on four post-breeding female northern elephant seals, jointly with ARGOS satellite transmitter and head-mounted camera, to determine their migration paths and prey type respectively.
We found that most dives were foraging dives (80-90%), meaning that seals foraged continuously day and night at a mean depth of 507-562m, with an apparent daily pattern in foraging depth, deep by day and shallow at night. Our estimation of prey size suggested that seals foraged on very small prey such as lantern fish by suction feeding (i.e. they swallowed prey whole) in the mesopelagic zone (200-1000m).
Our results suggest that the mesopelagic layer of the northeast Pacific Ocean provides an important habitat for this seal. The broadly distributed migration paths of this seal revealed by previous studies also suggest that much of this ocean provides prey for seals, indicating that prey are distributed rather evenly at low density rather than densely spaced in particular areas.
Although toothed whales use echolocation buzzes to search for prey remotely, seals are not able to sense prey remotely. Therefore we hypothesize that seals employ repeated deep diving to maximize encounters with prey in the mesopelagic zone.
Image caption: Northern female elephant seals at colony.
Special Feature: Mechanisms of Plant Competition
Joseph M. Craine and Ray Dybzinski
For millions of years, plants have struggled with one another to acquire the basic resources needed to grow and reproduce. Competition for nutrients, water, and light, sustained over millions of generations, has shaped plants in ways we are only beginning to understand. The unique properties of each type of resource have led to unique sets of adaptations associated with competition for these resources. Competition for light and nutrients has selected for the ability to preempt the supply of these resources from competitors. Competition for light selects for plants that grow taller faster and hold more leaves than is optimal, denying light to potential competitors below. Competition for nutrients selects for plants that produce more roots than is optimal, which ensures that nutrients come in contact with their roots before competitors. These adaptations might not allow them to maximize their productivity in the absence of competition, but they do ensure success in a competitive environment. That is, competition may select for better competitors, but not necessarily for plants that are more efficient or more productive.
Competition for water, as far as we know, selects for similar adaptations as does surviving drought: withstanding immense tensions on internal water caused by drying soils. In all, understanding how plants compete for nutrients, water, and light is a key to understanding the diversity of life on earth and how resources are utilized by plants. As some resources are likely to become scarcer in the future, understanding how plants compete for resources holds promise for improving agriculture and maintaining the ecosystem services provided by plants worldwide.
Image caption: Root system of a North American perennial grass, Schizachyrium scoparium, a good competitor for nitrogen.
Scott Burgess, Michael Bode, and Dustin Marshall
A mother usually only has a finite amount of resources to devote to her offspring. Mothers therefore face a trade-off between fewer, larger offspring, or more numerous, smaller offspring. The optimal balance between the size and number of offspring a mother should produce depends on how much fitter a larger offspring is compared to a smaller offspring.
Most studies addressing the offspring size-number problem typically focus on habitat quality. That is, studies typically assess how factors like food availability, competitors or predators influence the relative fitness differences between small and large offspring. In many species, offspring must disperse away from their parents before the effects of habitat quality can be seen. Such dispersal is often energetically or physiologically demanding. We predicted that smaller offspring with fewer resources might not have the stamina to survive after finally reaching distant habitat compared to larger offspring with more resources.
In essence, we show that habitat spacing may be just as important as habitat quality. After experimentally delaying settlement in a marine bryozoan (Bugula neritina), we showed that smaller larvae had lowered post-settlement performance compared to larger larvae. This is probably because the energy a mother gives to smaller offspring is used to prolong the larval stage at the expense of being used by offspring for growth and development after colonization. Larger offspring, on the other hand, may have more ‘fuel in the tank’ to cope with the energetic demands of dispersal.
We combined these empirical results with a mathematical model of a size/number trade-off and dispersal in idealized ocean currents. Together, our results show that more-isolated habitats favor mothers that produce larger offspring, rather than mothers that produce many offspring. Producing many offspring (and hence smaller offspring) increases the chance that at least some offspring reach distant habitat. However, producing many offspring is of little use when smaller offspring do not survive well once they arrive at distant habitat.
In nature, the better-studied features of habitat quality will likely impose selective pressures on how mothers provision their offspring in addition to habitat spacing. What we have done in this paper is to isolate and characterize a previously overlooked component of the overall selective pressures likely to act on offspring size and number in nature.
Image caption: Close up of a section of marine bryozoan (Bugula neritina) showing the specialized brood chambers (white spheres) in which a single embryo develops before being released as a larva into the sea. The filter-feeding structure (lophophore) of each zooid can also be seen.
Eric E. Flores, Martin Stevens, Allen J. Moore and Jonathan D. Blount
Many prey species have defences such as toxins or spines, and make use of colouration and patterning to warn off predators; this association between signalling and defence is known as aposematism. However, juveniles of aposematic species may become conspicuous before they possess an effective defence, which might be expected to place them at increased risk of predation. Such conspicuousness may be influenced both by aposematic colouration and variation in body size, brighter and/or larger individuals being more discernable to predators. Attaining large body size may itself be favoured by natural selection, because bigger individuals are likely to have greater energy reserves and foraging capacity in early adult life. Therefore, how juveniles of aposematic species optimise their development in terms of body size and warning colouration is unclear. We reared green and black poison frog (Dendrobates auratus) tadpoles on a relatively low or a higher food supply until metamorphosis, and tested the hypothesis that individuals with more resources should maximise their growth while reducing their investment in warning signals. Metabolically intensive activities such as growth might be expected to incur costs at the physiological level, resulting in a trade-off between growth and signalling. Therefore, we also measured physiological condition in terms of markers of antioxidant activity and oxidative damage, and assessed how this related to signal expression. We found that low-food froglets were relatively small, and their body size and signal luminance (perceived brightness) were positively correlated. In contrast, in high-food froglets body size and warning signal luminance were negatively correlated. This reduction in warning signalling in relatively large, high-food froglets was not significantly associated with markers of oxidative balance, suggesting that this was not a consequence of a resource allocation trade-off. Rather, it appears that larger froglets facultatively reduced their investment in warning signalling. Such a strategy seems likely to have evolved in order to minimize predation risk during the vulnerable period early in life when individuals are warningly coloured but as yet lack sufficient defences to protect them against predators.
Image caption: Green and black poison frog (Dendrobates auratus).
Special Feature: Mechanisms of Plant Competition
Clare J. Trinder, Rob W. Brooker and David Robinson
The study of plant competition is controversial. Although it has been studied for over a hundred years, researchers still find it hard to agree on a general set of rules that predict which particular plant will win in different habitats; under different environmental conditions (hot or cold; dry or wet) or when soil nutrients are plentiful or scarce. We suggest that these difficulties arise from the way that we have been studying plant competition. Early competition experiments focussed on agricultural crops and the impact of weed species on final yields. The approach of measuring final yield (as the weight of plant material or its seed output) persists today, even when studying wild plants in the natural environment. From our own work measuring competition between two common grassland plants (ribwort plantain and cocksfoot grass), we found we could interpret our results by studying their growth across the whole summer. We found that at earlier stages of their development plantain was the stronger competitor but later on cocksfoot overtook it and become the winner in this contest for soil nitrogen – a key plant nutrient. From this we realised that the length of time that a plant competition experiment runs for could completely change the outcome of the experiment. In our case, an earlier harvesting date would have shown plantain as the winner, but a later harvest showed cocksfoot as the superior competitor. With this in mind, we urge other researchers to consider plant competition as dynamic, changing through time, rather than a static process with an easily defined end point which tells us all we need to know about the competitive interactions between the plants. We also discuss whether it is appropriate simply to measure the weight of plants at the end of an experiment. We suggest that we should be developing methods to allow us to measure the uptake of resources that plants compete for directly, such as soil nutrients, as plant weight is likely to reflect a range of factors in addition to its ability to take up nutrients before its competitors are able to.
Ribwort plantain and cocksfoot grass grown in competition.
Franck A. Hollander, Nicolas Titeux and Hans Van Dyck
There is accumulating evidence that human-altered environments may attract organisms to habitats associated with low reproductive performance, thereby leading to an ‘ecological trap’. However, few studies examining the existence of ecological traps have dealt with the mechanisms underlying the preference for a low-quality habitat. To do so, the key ecological conditions and resources determining habitat preference and habitat quality must be compared between different habitat types used by a species in the same study area.
In the present study, carried out in southern Belgium, we examined whether between-habitat differences in food availability and food use might explain an ecological trap in the red-backed shrike (Lanius collurio), an insectivorous farmland bird that was recently shown to prefer a low-quality habitat (open areas in plantation forests, low reproductive performance) over high-quality habitat (farmland, high reproductive performance). Based on the sampling of invertebrate items used by the shrikes to feed their offspring, we showed that food for the shrikes was considerably less abundant in the forest habitat associated with the highest preference. Although larger prey items were available in forest, parent shrikes failed to feed their offspring with larger prey items than in farmland habitat. Parent shrikes delivered food to their offspring more often in farmland and this higher rate of nest visits induced better condition of the nestlings than in forest. Evidence of strong among-nestling competition for food was also found in forest only, suggesting that competition between kin for the same food resources in the nests was only apparent in the preferred habitat.
Altogether, these results demonstrate the existence of food limitation for an organism subject to an ecological trap. Shrikes were shown to be unable to correctly predict and deal with the environmental conditions in terms of food availability during the breeding period in the preferred forest habitat type. We suggest that dynamic environments under intense human use may involve a biased perception of habitat quality relative to food availability and may cause maladaptive habitat selection. This might especially be the case in mobile and time-stressed organisms that allocate only a limited time budget to settlement decision-making, with potentially negative consequences for the conservation of such organisms.
Image caption : A male Red-backed shrike delivering food to its offspring in forest habitat. Photo credit : Franck A. Hollander.
Zachary C. Zuckerman and Cory D. Suski
Reproductive success is critical for the passing-on of genes to offspring, and for maintaining viable population sizes. To maximize reproductive success, species from a wide variety of animals- from spiders to primates- provide care for their offspring. For care-providing species, though, not every reproductive bout is successful. Determining the mechanisms driving failed reproduction is integral to understanding the threats to a species, and provides insight into what limits good parenting in the animal kingdom.
Certain aspects of parental care have been well studied, and their impacts on reproductive success well documented. For instance, caring for offspring can be stressful, and nutritional condition can limit the energy available for a parent to invest in care. To better understand parental investment, the current study used a brood-guarding fish, the largemouth bass, as a model species. Parental stress, nutritional condition, number of offspring, offspring age, oxidative stress (the ability of an individual to neutralize cellular damage-causing reactive oxygen species ), and parental hormone condition were compared against the threat of offspring depredation in their effect on nesting success.
Researchers conducted snorkel surveys in shallow water of a lake in Canada, observing largemouth bass on their nests. The fish were then captured, blood collected for physiological analysis, and the fate of the nest (successful or not) tracked. Results indicate the strongest driver of nest failure was the density of brood predators- in this case, high densities of bluegill and pumpkinseed sunfish in the vicinity of unsuccessful nests- independent of the occurrence of depredation. In addition to brood predator density, unsuccessful nests had more developed offspring at the time of capture, and fewer offspring in the nest.
These findings suggest that the leading theories for factors driving parental care- in particular, parental stress, nutritional condition, and hormone condition- when considered along with biotic nest environment, may not be the most important determinants of reproductive outcome. Additionally, these findings provide new evidence as to how predators can directly influence reproductive success in wild organisms, without actually preying on offspring. This finding has implications for the ecological impact of anthropogenic disturbances (e.g., urban sprawl, habitat fragmentation , and predatory invasive species), and the ability of parental care-providing organisms to avoid high-risk areas to raise young.
Image caption: A male largemouth bass (Micropterus salmoides) guards his bowl-shaped nest. Eggs are visible as white dots on the vegetation and woody debris. Photo credited to Julie Claussen.
Graeme C. Hays and Rebecca Scott
How far can various animals migrate ? This question has intrigued biologists for many decades, but historically migration distance was often difficult to measure. However, over the last 20 years several techniques have been developed to record migration distances. For larger animals, direct satellite tracking is now feasible and allows individuals to be followed for many months or even years. For small animals, molecular approaches allow their point of origin to be determined. We examined published studies on migration distances recorded in these ways for > 5000 sea turtles of 5 species. For hard shelled turtles, the migration champions were green turtles that breed at Ascension Island (a remote island in the middle of the Atlantic) and feed on the coast of South America. However, their one-way migration distance (circa 2,850 km) was dwarfed by the huge distances (>10,000km) travelled by juvenile turtles as well as a species of soft-shelled turtle, the leatherback. In contrast to adult green turtles, both these groups feed during their oceanic crossings and this allows them to travel across the widest oceans. Adult green turtles, on the other hand, fast during their oceanic crossings and so the maximum fuel store (i.e. how much fat they can carry) seems to limit their migration distance. For adult turtles, their migration distances are similar to equivalent sized marine mammals and fish (e.g. seals and sharks). However, for juvenile turtles, their maximum migration distances are well beyond those expected for equivalent sized marine mammals and fish, but less than those found in some similar sized birds. Birds can accomplish their huge migrations (>15,000 km) by travelling quickly so that their fuel supply (fat) is not exhausted.
Image caption. Some sea turtles travel across the widest oceans. Photo provided by Gail Schofield, Department of Biosciences, Swansea University.
Cédric Frenette-Dussault, Bill Shipley and Yves Hingrat
Ecologists tend to study the natural world in separate compartments: plants, animals, fungi or bacteria, but seldom do we study two or more of these large groups simultaneously. This could lead us to underestimate the importance of the numerous interactions that can take place in natural ecosystems, thus limiting our understanding of ecosystem functioning. Thus, it is important to consider these interactions when studying components of ecosystems, as they are fundamental. To develop our understanding, we need models that can make predictions of how the natural world could evolve in a changing environment. This is especially relevant considering a largely accepted climate change scenario where increasing temperatures might strongly affect our environment. As an example, climate change simulations in arid ecosystems suggest an increase in aridity, which might lead to severe desertification. This could have strong negative effects on plant and animal survival, but also on local human populations’ economies that are partly based on traditional herding. Thus, being able to predict the changes to come over the next decades in these ecosystems is an advantage, as it would allow us to suggest efficient ways to mitigate the impacts of climate change, and ensure better conservation of natural resources. But before we can come up with sophisticated conservation plans, we must first have a better understanding of the interactions between plants, animals and their environment.
In this study, we looked at the relationships between plants, ants and environment in the arid eastern Moroccan steppes, by measuring various characteristics (i.e. what are called functional traits) of plants and ants. These functional traits are appropriate for those interested in understanding how organisms and communities function and adapt to environmental conditions. With this information, we were able to identify how each compartment of the ecosystem is related to the others. In a few words, we found that changes in the characteristics of the environment will drive changes in the vegetation, and that ant colonies will be affected through these changes in plants, but not necessarily directly by changes in climate. This is a simple model that can guide us when deciding what actions to prioritize, depending on conservation targets.
Image caption: The steppe ecosystem near Missour, eastern Morocco. Photo by Cédric Frenette-Dussault.
Daniel González-Tokman, Isaac González-Santoyo and Alejandro Córdoba-Aguilar
Reproduction is a priority but also a costly business and any energetic investment into reproducing will affect investment in other non-reproductive traits. However, the cost for any individual may vary depending on its age. This is explained by an animal’s perception of mortality. For example, a relatively old animal will face a higher cost if he/she decides to invest more in reproductive traits compared to a relatively young animal. The reason for this is that an old animal has less energy than a young animal. What would happen to investment in reproduction if, say, animals of different age also need to invest their energy in something else (for example, resisting an infection)? According to the above reasoning, old animals will invest more energy in reproduction than young animals. However, since old animals have less energy than young animals, the former are likely to die sooner.
The evidence for these predictions is so far incomplete so in our study we set out to investigate them. For this we used males of a territorial damselfly which were studied in their natural habitats. We had four groups: infected young males, non-infected young males, infected mature males, non-infected mature males. To simulate an infection, we inserted a nylon filament into the body. After manipulation, we recorded all males’ territorial behavior and mating success, as well as physiological non-reproductive traits. We found that infected mature males defended territories for longer, were more aggressive and gained more matings than infected young males. However, these advantages came with a cost: infected mature males ended up with less fat stores than infected young males. All this corroborates the view that at an advanced age and when life chances are reduced, males will invest more into reproductive traits than young males, but the former will pay a higher energetic cost.
Image captions: Damselfly illustrations by Barrett Klein, originally published in Abbott (2011).
Special Feature: Plant-Microbe-Insect Interactions
Plant-feeding by insect vectors can affect life cycle, population genetics and evolution of plant viruses
Serafín Gutiérrez, Yannis Michalakis, Manuella Van Munster & Stéphane Blanc
All pathogens are exploiting their host’s resources, sometimes exhausting them completely. Inevitably, sooner or later the host will die, forcing the pathogen to move on and find other healthy individuals to ensure further development, reproduction and spread. Plant viruses cannot move from host to host autonomously, and can only leave and enter hosts through breaks in the pectin/cellulose cell wall. The use of insect vectors is a common strategy for the transmission of viruses and the three partners, plant, virus and insect vector, have developed intricate interactions with important ecological implications.
It is now proven that plant viruses can influence the physiology and behavior of insect vectors, in a way that increases their chances of transmission. For example, a viral infection can induce changes in plant properties which in turn speed up the development of insect vectors, increase their reproduction or even augment the proportion of migrating individuals that can spread the virus more efficiently. Some plant viruses can also infect their insect vectors and similarly but more directly impact on their physiology and behavior.
In contrast, no information is available on possible reciprocal interactions, where the insect vector attack on an infected plant would induce a specific change in the infection cycle of the virus, its phenotype, or even its population genetics, evolution and epidemiology. In this review, we focus on these overlooked interactions by speculating, based on the rare hints available in the current literature, on unforeseen aspects related to i) the impacts that the feeding habits of different insect vectors can have on the evolution of plant viruses, and ii) the possibility that a plant stress induced by an insect vector can be perceived by a virus as a signal for a major switch in its infection cycle, triggering specific modifications within the infected host plant that affect primarily the efficiency of vector-transmission.
Image caption: An aphid is feeding on a plant leaf infected by two variants of a virus species, respectively labeled by a green and a red fluorescent protein. This image illustrates a complex interaction between the host plant, the virus and the insect vector. Depending on the respective location of the viral variants within the host plant, so on the plant-virus interaction, and on the feeding behavior of the insect on this plant, so on the plant-insect interaction, the outcome of the virus-vector interaction can be utterly different. The aphid drawing is by Nicolas Sauvion (INRA, France). The photo of the leaf is by Serafìn Gutierrez and Elodie Pirolles.
Better keep in shape: importance of being big and fat to use energy saving strategies in mouse lemurs
Pauline Vuarin, Melanie Dammhahn and Pierre-Yves Henry
Biodiversity is actually threatened by global changes, thus understanding how organisms respond to these changes is of major interest in ecology. In this context, energy saving strategies employed by a variety of organisms are powerful and efficient measures to deal with environmental constraints. However, these strategies remain poorly understood. The grey mouse lemur (Microcebus murinus), a small nocturnal primate inhabiting the dry forests of western Madagascar, represents a good model to study these questions. To face the energetic constraints found in their natural habitat (decrease in food availability and in ambient temperature during the dry season), the grey mouse lemur can enter into torpor, a strategy close to hibernation, which allows a reduction of energy expenditure thanks to a reduction of body temperature, metabolism and activity. Based on a field survey of free ranging grey mouse lemurs, our study aimed to investigate which factors constrain the expression of torpor in this species. At the onset of the dry season, we monitored air temperature as well as skin temperature of 14 free-ranging individuals of known body mass and size. In accordance with previous studies, we found that ambient temperature affects torpor use, torpor depth increasing with decreasing ambient temperature. Nonetheless, behind this already documented effect of ambient temperature, we also demonstrated that both body size and body condition (i.e. an index of energy body reserves) constrain torpor use. Fatter or larger mouse lemurs expressed deeper torpor than lean or smaller ones. Furthermore, larger and/or fatter mouse lemurs had a greater propensity to express torpor, and a greater flexibility in its expression, meaning that they were able to adjust torpor use to variations in ambient temperature. Hence, our study illustrates that in a single population, different strategies co-occur, with body size and condition being the key determinants of the energy conservation strategy that an individual will adopt. Such studies are needed to predict to what extent organisms will be able to overcome environmental constraints, especially in the context of global changes.
Image caption: Female grey mouse lemur (Microcebus murinus) in Kirindy forest, western Madagascar (photograph by Pauline Vuarin).
Zachary R. Stahlschmidt, Njal Rollinson, Madison Acker, and Shelley A. Adamo
You may find field crickets to be annoying household pests, but they have to deal with problems similar to those faced by all animals — even humans. We regularly make choices between important life components, such as when we divide our paycheck between groceries and rent, and so do crickets. For example, they make choices about how to divide their efforts between egg production and immunity (i.e. resistance to pathogens). We wondered, if crickets are forced to spend resources on immunity due to repeated immune challenges, do they reduce the number and/or quality of offspring? We also wondered whether food availability affected this tradeoff between reproduction and immunity—that is, if crickets have unlimited food resources, can they adequately fuel both reproduction and immunity? Previous researchers have investigated these questions by examining individual aspects of reproduction, such as the size of ovarian follicles, and often during a single breeding season. We expanded on this work by examining the effects of immune challenge on both the number and quality of offspring produced over females’ entire lifetimes, because these aspects of reproduction better reflect the fitness consequences of immune challenge.
We studied the tradeoff between reproduction and immune function in adult Texas field crickets, which are found in the south-central U.S. and are short-lived (adults live < 1 month in their natural habitat). In this species, a tradeoff between reproduction and immunity was obligate or independent of resource availability because immune challenge reduced the number of eggs and hatchlings that crickets produced over the course of their lives regardless of food availability. Crickets with unlimited food produced more and larger hatchlings than crickets with limited access to food, but neither food availability nor immune challenge affected other aspects of offspring quality, such as egg size or hatching success. We observed a tradeoff between offspring quality and number. That is, crickets that produced relatively few hatchlings had hatchlings that were relatively large and robust. By demonstrating that not all eggs are created equal, we provide key insight into the fitness tradeoff between reproduction and immunity.
Image caption: Texas field cricket (Gryllus texensis) laying eggs into moist cotton substrate. Photo by Z. Stahlschmidt.
Special Feature: Mechanisms of Plant Competition
Stephen P. Bonser
Competition among neighbours for limited resources is one of the main adversities most individuals must deal with in natural communities. Being denied resources by neighbours has a suite of negative effects on individuals including reduced survival, slower growth, and fewer offspring. For over 40 years, scientists studying competition in plant communities have assumed that plants faced with severe competition should respond by being better competitors. In other words, plants under competition should delay reproduction in favour of more effectively acquiring resources. I tested this prediction by examining previously published studies on how plants grow and reproduce when grown in competitive conditions. Contrary to the long standing assumption on how plants are believed to respond to competition, I found that increasing the severity of competition was related to increased rather than decreased allocation to reproduction. This finding was the same for both short lived weedy annual species, and longer lived perennial herbs. It appears that severe competition is a harbinger of death in plant communities, and plants employ a strategy of increased reproduction prior to dying under severe competition. Greater allocation to reproduction in weedy annual plants under competition demonstrates that these plants have adapted to life in competitive environments. This finding challenges the long standing assumption in ecology that competition is unimportant in highly disturbed weed-dominated communities. Greater allocation to reproduction under strong competition in longer-lived perennial herbs suggests that these plants tend to give up rather than fight when faced with impending mortality. Plants with a strong ability to compete against their neighbours do evolve but, somewhat paradoxically, they likely do so under low or modest competition. The research I present here presents new ways of thinking about how plants adapt in their struggle for existence.
Image caption: Photo credited to Angela Moles.
Special Feature: Plant-Microbe-Insect Interactions
David Giron, Enric Frago, Gaëlle Glevarec, Corné M.J. Pieterse and Marcel Dicke
Plants are abundantly present on Earth and constitute key nutritional resources for many organisms. As such, under pathogen infection and/or herbivore attack, plants have to mount a defensive response which specifically targets the invader. As the amount of nutrients available to plants is often limited, defence responses usually come at the cost of other metabolic functions such as plant growth.
While pathogens and herbivorous insects can inflict severe damage on plants, other (micro)organisms may however offer great benefits by providing for example key nutritional resources. In this context, plants have to find a way to defend themselves against attackers with an appropriate defensive response while facilitating beneficial organisms.
A key step in these intricate plant-microbe-insect interactions is recognition of the invader and activation of a suitable plant response. Specific plant molecules such as phytohormones are chemical mediators involved in these two crucial processes. It is also interesting that plant growth and defence can be regulated by similar phytohormones allowing plants to finely balance protection against aggressors and acquisition of benefits/growth.
Over the course of evolution these phytohormones may have been the target of herbivorous insects and pathogens to hijack plant metabolism, control its physiology and/or morphology and successfully invade the plant. In the case of insects, manipulation of the plant may rely on their specific association with bacteria hosted within the insect's body which allow them to produce key phytohormones disrupting the plant defence response and diverting plant nutritional resources towards the insect feeding site.
Cytokinins are plant hormones that play an important role in plant morphology, plant physiology and plant defence. They are involved in numerous plant-pathogen and plant-insect interactions and strongly impact not only plant growth and defence but also the whole community of insect and pathogen species sharing the same plant by facilitating or preventing plant invasion. This suggests that cytokinins are key regulators for successfully invading a host plant, and highlights the complexity of the finely-balanced responses that plants use while facing both invaders and beneficial organisms.
Image caption: Caterpillars use bacteria to prevent leaf senescence in autumn. The phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts to manipulate the physiology of its host plant resulting in a 'green-island' (insect feeding area) where plant tissues remains green and photosynthetically active while the remaining leaf tissues undergo leaf senescence (Credits: Mélanie Body).
Special Feature: Plant-Microbe-Insect interactions
Ana Pineda, Marcel Dicke, Corné M.J. Pieterse and María J. Pozo
Plants in nature interact with harmful organisms such as herbivorous insects and microbial pathogens, but also with beneficial organisms, such as beneficial fungi and bacteria and carnivorous insects that kill the herbivores. Additionally, plants are exposed to multiple abiotic stresses such as nutrient deficiency and drought. Exciting advances highlight that plants have an immune system with interconnected signalling pathways that regulate the interactions with beneficial and detrimental organisms, as well as the plant responses to abiotic stresses. By understanding how biotic and abiotic factors affect the activation of these pathways, we may be able to predict how plant-microbe, plant-insect and plant-microbe-insect interactions will respond to a changing environment.
Beneficial microbes such as rhizobacteria and mycorrhizal fungi can promote plant growth, as well as help plants to tolerate abiotic stress and "“deal"” with pathogens and herbivorous insects by inducing systemic resistance (called ISR) . Therefore, beneficial microbes may play an important role in agricultural and natural ecosystems in a changing environment, where abiotic and biotic stresses are expected to increase. However, the effects of beneficial microbes on herbivores are highly context-dependent, with a range of positive and negative effects. A major question is what the reasons are for these conditional outcomes, and recent evidence shows that abiotic stresses such as changes in soil nutrients, drought and ozone can modify the outcome of plant-microbe-insect interactions.
Here, we review how abiotic stress can affect plant-microbe, plant-insect and plant-microbe-insect interactions, and the role of the plant signalling pathways in regulating such interactions. Most studies show that the effects of microbes on herbivores are strengthened under stressful conditions. We propose that, at least in part, this is due to the cross-talk of the plant signalling pathways, that is when a signal in one pathway has an effect on another pathway. We also propose that microbes can help plants to deal with insects mainly under challenging conditions that compromise an efficient activation of plant defences.
In the context of global climate change, it is crucial to understand how abiotic stresses will affect species interactions, especially those interactions that are beneficial for plants. The final aim of this review is to stimulate studies unravelling when “"beneficial” " microbes really benefit a plant.
Image caption: Carnivore insect ready to parasitize a caterpillar. Image courtesy of Tibor Bukovinszky, Bugs in the picture.
Special Feature: Plant-Microbe-Insect Interactions
Thure P. Hauser, Stina Christensen, Christine Heimes and Lars P. Kiær
Plants are often attacked by insects and diseases, and each of these is known to cause substantial losses in agriculture, forestry and natural plant communities. The question we raise here is whether the combined losses to insects and diseases, when they co-infect the same plants, are more or less severe than the sum of losses when they attack the plants alone. Chewing insects may e.g. help pathogens to establish in plants through wounds, and either may suppress plant defences, which may sometimes benefit both insects and pathogens. Whether this leads to more severe losses and decreased plant yield, compared to when the insect and pathogen attack on their own, is still little studied. This is unfortunate, as such knowledge may allow e.g. better pest control in agriculture. We therefore combined the results from previous studies, and analysed whether we could find general patterns in the combined impacts on plants, e.g. among different groups of insects and pathogens. We also tested whether patterns suggested by other authors could indeed be found in our larger data set.
Surprisingly, none of the patterns suggested by others, based on interactions among certain feeding types of insects and diseases, seem to hold across the studies analysed. Instead, our results show that the combined impact of insects and pathogens is more synergistic and severe for attacked plant parts than for the plant as a whole. Thus, the plant may be able to compensate for local losses to some extent, resulting in a less severe combined impact on total biomass and yield. We also found that combined impacts on plants differ among different environments, again suggesting that resource levels of the plants may determine to what extent it is able to compensate for losses to insects and pathogens. Our results thus imply that it is complicated, and may turn out to be impossible, to make general predictions about combined impacts of insects and pathogens on plants; however, we need more studies to determine this.
Image caption: Plant leaf of winter cress attacked by both herbivorous flea beetles and white rust disease. Photo by Tamara van Mölken.
Special Feature: Plant-Microbe-Insect Interactions
Aspects of plant volatile emission in response to single and dual infestations by herbivores and phytopathogens.
Camille Ponzio, Rieta Gols, Corné M. J. Pieterse and Marcel Dicke
Though immobile, a plant under attack by pathogens or insects is far from defenceless. Plants possess several ways of defending themselves when attacked, such as producing plant odours, which are often referred to as induced plant volatiles. These are an important means of communication between a plant and other members of its community, such as other plants, herbivorous insects, pathogens, and beneficial insects. Until recently research focused on the interactions between a plant, one insect attacker and its associated beneficial insects. However, when there is more than one attacker on the plant the complexity of the interactions increases, and predicting the composition of the volatiles and their effects on the community is not so straightforward.
The production of attacker-induced plant volatiles is triggered by the activation of the plant’s immune system. Different types of herbivorous insects or pathogens will induce different branches, or pathways, of the immune system, leading to qualitative and/or quantitative alterations in the volatile blend. However these pathways can interact with each other by enhancing or reducing each other’s action. In the latter situation, activation of one pathway can block the activation of another needed for a defence response against a specific aggressor.
As a result, plants harbouring several insects and/or pathogen aggressors can emit volatiles that make the plant more (or less) attractive to other herbivorous insects, or prevent a pathogen from developing. Similarly, beneficial insects may be much more or less attracted to plants that have their host/prey and another attacker on them, than to plants with only their host or prey present. This large amount of variation may be explained by numerous factors, making it difficult to discover general patterns in plant responses to multiple attack and the mechanisms underlying them. Different combinations of plant, insect and pathogen species may interact differently, which may affect the plant’s response and its ability to defend itself. For example, the number of attackers, their location on the plant and the order in which they attack can also have sizeable effects. In short, as we learn more about interactions involving multiple attackers, it becomes clear that we are still far from fully understanding the mechanisms involved.
Image caption: The parasitic wasp Cotesia glomerata, parasitizing on 1st instar larvae of the large cabbage white butterfly, Pieris brassicae. Photo by Hans Smid / Bugsinthepicture.com
Special Feature: Responses to global climate change: Insights from organismal physiology
Michael R. Kearney, Stephen J. Simpson, David Raubenheimer and Sebastiaan A. L. M. Kooijman
Having enough food and water, and staying within comfortable temperatures, are basic life requirements for all animals. If we can accurately predict the degree to which animals can regulate their heat, water and nutritional levels in different environments, we can begin to understand how environmental change will affect biodiversity. In this paper we show how principles from the fields of thermodynamics and animal behaviour can be integrated to understand how animals jointly balance their heat, water and nutrient budgets.
Thermodynamics is the field of physics that concerns the flows of energy and matter. In animals, the flows of heat, water and food are intimately connected. We show how principles developed within the field of ‘biophysical ecology’ for considering heat flow can be connected with principles developed in ‘metabolic theory’ for understanding flow of energy and matter associated with food. In particular, we apply one of the most comprehensive and long-standing metabolic theories, the ‘Dynamic Energy Budget’ theory, to this problem and show how it can be integrated with ‘biophysical ecology’ to work out, jointly, the heat, water and food budget. The set of environmental requirements for an organism to survive and reproduce are called its ‘niche’ and in this article we propose the term ‘thermodynamic niche’ to cover core heat, water and food requirements.
A key issue in determining thermodynamic niches is that animals don’t passively experience their environments. Rather, they use behaviour to try and find their thermodynamic niches. We show how the principles of the Geometric Framework of Nutrition can be used to understand the consequences of different behavioural choices for what to eat and where and when to forage. We demonstrate the approach using the example of an herbivorous lizard, illustrating the potentially strong tradeoffs that exist in balancing heat, water and food budgets, even in ‘dry-skinned’ animals. Such ‘thermodynamic niche’ models will enable physiological ecologists to make predictions of the responses of animals to future environmental change.
Image caption: Egernia cunninghami photo by lostandcold at flickr
Special Feature: Mechanisms of Plant Competition
Bradley J. Butterfield and Ragan M. Callaway
Plants can have both positive and negative effects on one another. A great deal of research has been conducted on the mechanisms and outcomes of competition, such as how neighboring plants suppress growth and reproduction of competitors by reducing light or nutrients. Some of this research has also asked whether specific traits contribute consistently to the ability to compete well, generally traits that determine how plants respond to and influence their local environment. What is less well understood is how such traits influence the outcome of positive interactions among plants. Positive interactions, or facilitation, are a consequence of plants modifying their microenvironment through positive feedbacks (e.g. enhanced soil fertility, herbivore deterrence, reduced temperature extremes) or increasing the availability of a limiting resource for other species (e.g. facilitation of grasses by deep-rooted trees that reduce evaporation from shallow soils through shading). Why certain species benefit from neighbors while others do not, and why some species are good nurse plants and others are not, is likely strongly influenced by their functional traits. However, we know very little about which traits determine the outcome of facilitative interactions, or whether a suite of similar traits are important across the broad array of environments in which facilitation occurs.
In this study, we reviewed the literature on how functional traits respond to a range of environmental factors, and related these responses to the facilitative effects of neighbors. We used this comparison to predict why certain species may benefit from neighboring plants and others may not. We focused on three frequently measured traits: specific leaf area (the ratio of leaf area to dry mass), height and seed mass. We found that predicted facilitative responses of plants fell into two general categories, depending on whether neighbors buffered dynamic fluctuations in environmental stresses, or ameliorated persistent stresses. While these predictions need further testing, the trait-based patterns presented here provide useful generalizations for how plants may influence biodiversity through positive interactions, as well as identifying commonalities in the mechanisms of positive interactions across seemingly disparate environments.You can also listen to Alan Knapp's podcast interview with Brad Butterfield via Soundcloud:
Image caption: Facilitation of Potentilla, Erigeron and Aquilegia sp. by Silene acaulis in the Rocky Mountains, and Atriplex confertifolia by Ephedra torreyana in the Great Basin Desert. Do similar functional traits determine facilitation in these very different environments?
Special Feature: Mechanisms of Plant Competition
Ronald Pierik, Liesje Mommer and Laurentius ACJ Voesenek
The vast majority of plants grow in high densities and compete for resources. Aboveground, plants compete for light, whereas below-ground competition occurs for the various mineral nutrients and water. Species can differ in their growth rates and resource acquisition. In addition plants can be plastic in their resource acquisition in response to competition. In order for plants to optimize their behavior in response to neighbouring competitors, these neighbours first need to be detected.
Plants can detect their neighbours aboveground through changes in light quality and quantity. Particularly the red:far-red light ratio is reliably reduced due to far-red reflection by neighbouring leaves and red light absorption for photosynthesis. This neighbour detection occurs even before competition sets in, thus preparing plants optimally for the struggle for resources. Additional aboveground signals to detect neighbours include volatile organic compounds that are produced and released by neighbouring plants and even touching of neighbouring leaf tips. In response to these signals plants invest more in vertical elongation of their shoots as part of the so-called Shade Avoidance Syndrome, which positions the photosynthesizing leaves higher in the vegetation, i.e. closer to the light.
Belowground, neighbouring plant roots alter water and nutrient availability and these changes can serve as cues to detect competitors. The root system architecture of most species is highly plastic and can be modified to localize the majority of the roots in nutrient-rich zones so as to maximize nutrient capture. In addition to taking up water and nutrients, roots also excrete a rich variety of water-soluble exudates. These exudates may have direct affects on neighbouring plants. They may for example be toxic and reduce growth of nearby competitors. These exudates will also affect the community of microbes that live in the soil zone directly around the roots systems (called the rhizosphere), which may have indirect effects on interactions with competing neighbour plants.
Our review argues that understanding the mechanistic aspects of plant neighbour detection and plasticity is key to exploring ecological interactions, generating hypotheses and understanding constraints in plant competition.
High density field of plants. Image courtesy of the authors.
Special Feature: Responses to global climate change: insights from organismal physiology
Morgan W. Kelly and Gretchen E. Hofmann
Atmospheric carbon dioxide (CO2), produced by the burning of fossil fuels, is being taken up in large quantities by the world’s oceans. Dissolved CO2 produces carbonic acid and decreases ocean pH, a process known as ocean acidification (OA). This process leads to a reduced concentration of carbonate ions, which are used by many marine species to build calcium-based shells and skeletons. Laboratory experiments simulating future ocean conditions have shown negative effects of OA on many species, including effects on growth rates and reproduction. However most of this research has exposed modern populations of organisms to conditions not projected to occur until the next century. And yet we know from previous examples of human-caused environmental change, that natural populations of organisms can sometimes evolve quite quickly in response to a changing environment.
In this paper, we review the status of current scientific research on the potential for adaptation to OA in marine organisms. This body of work is currently quite small, but we argue that data on natural variation in pH, and lessons learned from previous work on adaptation to temperature, can shape the direction of future research. We conclude with a list of recommendations for future research priorities, and the technological tools for accomplishing these goals.
The current process of human-driven acidification is expected to produce changes in ocean chemistry more rapid than any experienced in the past 20 million years. Except for organisms with short generation times, the current rate of change will likely be too great for much adaptation based on new mutations to occur. However, given enough genetic variation in a species, substantial adaptation to environmental change is possible, even over a single generation. As a result, a priority in OA research for the next decade will be to document the extent of such variation and consider the role of evolutionary processes in projections about the effects of OA on modern marine species.
Image caption: Graduate Student Paul Matson samples water for pH measurements below sea ice in Antarctica
Special Feature: Mechanisms of Plant Competition
Angela Hodge and Alastair H. Fitter
There is growing but largely circumstantial evidence that micro-organisms can change the outcome of plant competition; direct evidence remains surprisingly scarce. Plants release substances from their roots that influence the microbial community in the soil around their roots creating a zone called the ‘rhizosphere’. Because different plants may release distinct cocktails of chemical substances from their roots into their rhizosphere, which will encourage certain microorganisms over others, they may support very different rhizosphere communities.
The best evidence that microbes can influence plant interactions comes from reasonably well characterised microbial groups that have close symbiotic relationships with plants, such as the arbuscular mycorrhizal fungi and nitrogen-fixing bacteria. However, because the majority of soil micro-organisms cannot be grown in the laboratory, making it difficult to devise manipulative experiments, there has been little progress in understanding how they may directly influence plant interactions. Consequently, most researchers have employed indirect approaches such as ‘plant-soil feedback’ studies, where soil, often sterilised, is conditioned by growing one plant species for a short time to cultivate a rhizosphere microbial community, after which a range of species is grown in the same soil and the impact upon plant growth followed. The consensus from these studies is that plant growth is more constrained by organisms present in their own rhizospheres than that of other plant species. This negative feedback is generally assumed to be due to a build up of microbial pathogens constraining plant growth in their ‘own’ soil, although pathogen populations are seldom measured. These ‘plant-soil feedback’ studies are also often characterised by short duration and small numbers of plant species.
Recent advances in new technologies now enable the mysteries of the soil microbial ‘black box’ to be unlocked and, if embraced, could open up new possibilities for rhizosphere manipulation and enhanced plant productivity as well as new insights into natural plant community drivers.
Image caption: external hyphae and spores of an arbuscular mycorrhizal fungus around a root. Image courtesy of the authors.
Special Feature: Responses to global climate change: insights from organismal physiology
Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field.
Luis-Miguel Chevin, Sinéad Collins and François Lefèvre
When facing strong environmental challenges such as those imposed by climate change, species may avoid extinctions by three main mechanisms: dispersal to their preferred habitat (or niche), genetic evolution in response to natural selection, or adjustment of the characters of the organisms at the individual level. The latter is termed phenotypic plasticity, and has received relatively little attention from ecologists and evolutionary biologists until recently. In this paper, we review the theoretical literature on how phenotypic plasticity and genetic evolution interact with population growth in changing environments. We describe models of plasticity, and how they have been used to generate quantitative predictions in a variety of contexts relevant to climate change. These include adaptation to a new environment following an abrupt change or introduction to a new habitat; responses to a sustained trend of change such as global warming; and adaptation to local conditions in the face of migration bringing locally maladaptive genes. We then assess to what extent these predictions can be tested with natural populations, and identify key difficulties in doing so, as well as possible ways to overcome them. Finally, we identify new questions that should be investigated in theoretical models. These questions arise from the examination of two emblematic cases of physiological effects of current climate change: resistance to drought and temperature extremes in trees, and responses to CO2 elevation in marine microscopic algae, the major carbon sink on earth. Our main conclusion is that proper understanding and prediction of the consequences of climate change for biological diversity requires taking into account the plastic responses of individual organisms, the evolution of populations, and their interacting effects.
Image caption: This forest of introduced cedars was used to study the variation in plasticity of radial growth in response to drought by one of the authors (F. Lefèvre).
Special Feature: Mechanisms of Plant Competition
Karl Niklas and Sean Hammond
Physical forces and chemical processes, such as the weight of snow or the rate of metabolism, invariably affect plant growth and the ability to cope with other neighboring organisms. The effects of these forces and processes on growth and competitiveness can be described mathematically in ways that can help ecologists understand how plants interact with one another, both competitively and cooperatively. Importantly, each mathematical description contains parameters that are physical constants (such as the acceleration of gravity), which no organism can alter. However, each description also contains parameters that can be changed as an organism moves, changes orientation, or grows in size (such as the surface area a plant projects toward the oncoming flow of wind or water). In addition, these mathematical descriptions involve the exchange of atmospheric gases (carbon dioxide and oxygen) and energy (primarily heat). Computer models show how these mathematical descriptions of mass and energy can help us to understand complex ecological phenomena such as species competition and co-existence, and community turnover in species composition. Collectively, these tools show that a critically important factor in understanding plant competition is how plants three-dimensionally display their surfaces to the physical environment, both above and below ground. For terrestrial and aquatic flowering plants, this involves the display of leaves. For aquatic algae, this involves the display of filaments or frond-like organs. An equally important factor is how this display of surface area changes over time as a plant increases in size. By considering a few fundamental physical laws and processes, much (but not all) of the ecology of plants can be explained and in some cases even predicted.
Image caption: Catastrophic snow loading on Arbor Vitae. Photo provided by Edward D. Cobb, Department of Plant Biology, Cornell University
Special Feature: Responses to global climate change: insights from organismal physiology
Ary A. Hoffmann, Steven L. Chown, Susana Clusella-Trullas
Cold-blooded animals including insects and lizards cannot survive and reproduce once temperatures become too high. These upper temperature limits tend to vary among species and also for different activities of animals. Typically limits are lower for reproduction than for survival, and higher for species that occur in deserts than those that are found in cool climate rainforests.
Here we ask whether upper limits are constrained in different ways. Can species evolve to change their upper limits, or are upper temperature limits relatively fixed in evolutionary time? To what extent can upper limits of different groups of species be affected by the environment? Answers to these questions are particularly pertinent today as global climate continues to warm. Average temperatures are now expected to increase by 2-4°C and extreme temperatures are expected to increase even further. This can threaten the survival of species if their upper limits are repeatedly exceeded.
To test for evolutionary constraints, we compare the upper limits across insects and lizards and consider whether related species tend to have more similar limits than unrelated species. If related species are more similar than unrelated species, this can point to a constraint. We suggest that this is likely to be the case, with limits pre-dating recent speciation events. Studies that have investigated genetic variation in upper limits within species also suggest that limits cannot be easily shifted through evolution via natural selection. This contrasts markedly with lower temperature limits that tend to vary much more among species and can be more easily changed by natural selection. We also point out that upper limits can be much less easily modified by the environment - such as through hardening - than lower limits.
As a result of these patterns, we suspect that many species could be facing extinction when the maximum temperatures in environments start to increase. Species will then need to move to cooler conditions if they are to persist. We suggest that this threat in both insects and lizards is greatest at mid-latitude locations rather than at the equator or at high latitudes.
Photo: A species of vinegar fly, Drosophila birchii, found in the wet tropics of Australia and New Guinea with an intermediate upper thermal limit when compared to other Drosophila species. This species and others from the tropics are exposed to high average temperatures but do not necessarily experience extreme temperatures like insects living in arid environments.
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