Lay Summaries Archive

Read Lay Summaries from previous volumes of Functional Ecology here:

Early View Lay Summaries

 

Cane toad impacts native species reproduction

Edward J. Narayan, Tim S. Jessop and Jean-Marc HeroCane toads present within terrestrial breeding habitats of the endangered Fijian ground frogs (Photograph by Dr Edward Narayan).

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Invasive species, major drivers of global change, cause unprecedented impacts on biodiversity. Their influence is most apparent on small oceanic islands where invasive species are the main cause of extinction. Understanding the mechanisms that make invasive species devastating is central to addressing their ecological impacts on the islands. One idea is that colonization of “simple” small islands affords invaders greater capacity to diversify and intensify their ecological roles beyond those seen in their native or invaded continental distributions.

Here, we used natural and manipulative field experiments to test if density-mediated competitive interactions from the highly-invasive cane toad could cause indirect effects and fitness loss to a small island population of the endemic and endangered Fijian ground frog. Over 13 successive monthly field surveys we collected 5000 non-invasive urine samples and measured body condition, survival and reproductive success of the Fijian ground frog. Samples were then analysed for reproductive and stress hormones. These data provided detailed accounts of how exposure to high-densities of cane toads caused major alterations in the nutritional status, physiological stress and reproductive physiology of ground frogs in both field enclosures and natural habitats. Most telling was that ground frogs in high toad density enclosures experienced extremely poor breeding success.

Despite a wealth of knowledge on the cane toad’s ecological consequences in invaded continents, such as Australia, our results reveal them to have extremely novel ecological roles and consequences on islands. Clearly, our results demonstrated how invasive cane toad competition, through extremely strong indirect effects, triggers major physiological changes that led to the reproductive collapse in Fijian ground frogs. Further, our study suggests it is important to limit alterations to island habitats to reduce the strength of invader-native species interactions. Thus, our results provide a striking example of why invasive species can disproportionately impact island endemics to potentially increase extinction risk.

Image caption: Cane toads present within terrestrial breeding habitats of the endangered Fijian ground frogs (Photograph by Dr Edward Narayan).
You can read the full article here.

 

Bacterial diversity enhances plant growth

Simone Weidner, Robert Koller, Ellen Latz, George Kowalchuk, Michael Bonkowski, Stefan Scheu and Alexandre JoussetPhoto of thale cress (Arabidopsis thaliana associated with bacterial community of Pseudomonas spp. (taken by Simone Weidner).

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In order to grow, plants need to take up soil minerals such as nitrogen. Nitrogen is however often limited and when present locked in the soil matrix. To make nutrients accessible to the plant, soil particles have to be broken down by enzymes. Since plants are not efficient in doing this themselves, they have to rely on soil microbes to make nitrogen available. To ensure an optimal nitrogen supply, plants “hire” soil bacteria by pumping huge amounts of sugars into the soil. By doing so, they attract and feed a dense bacterial community that in turn produces the required enzymes. Feeding bacteria is a huge investment for the plant and the effort is only worthwhile if bacteria do contribute to the required functions.

In this study we wanted to know how this function of making nitrogen available is influenced by the diversity of the bacterial community. We performed an experiment in which plants completely depended on the nitrogen supply from the bacteria and added bacterial communities to the plant that differed in their diversity.

Our study shows that bacterial diversity is an essential driver for the feedback of investment to the plant. Bacteria living alone produce less enzymes, slowing down nutrient cycling and plant growth. Mixing different species causes the bacteria to upregulate enzymatic activity, probably as part of a strategy to exploit resources better than their competitors. This helps to make more nitrogen available, and enhances plant growth.

Alterations of soil bacterial diversity, for instance by poor agricultural management, may thus have deleterious effects on plant growth. We propose that preservation of soil microbial diversity should be taken into account when it comes to agricultural management strategies. In addition, we propose that soil microbial diversity could be enhanced by reintroducing the missing species in order to improve nutrient mobilization and minimize the need for fertilizers.

Image caption: Photo of thale cress (Arabidopsis thaliana associated with bacterial community of Pseudomonas spp. (taken by Simone Weidner).
You can read the full article here.

 

Investigating isotopic functional indices to reveal changes in the structure and functioning of benthic communities

Carinne Rigolet, Eric Thiébaut, Anik Brind’Amour and Stanislas F. DuboisHaploops nirae, a gregarious tubiculous amphipod (crustacean) species (top picture) colonizing muddy marine sediments and engineering a unique habitat (bottom picture) while largely affecting associated species assemblages.

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The number of species is a key element for ecosystem functioning. However, not all species play the same functional role and/or respond to changes in the same way. Approaches to study species functions and interactions are mostly based on morphology (e.g. size, shape) or behaviour (e.g. feeding guild, motility). Using many such biological traits, one can calculate functional indices. They measure a potential functional niche of species assemblage (community). We suggest using stable isotopic compositions of species to provide a realized functional niche. Indeed, stable isotopes (i.e. 13C and 15N) in species’ tissues are directly linked with the species’ diet. As a result, they reflect information about the use of the physical habitat (e.g. size, hydro-climatic conditions) and the use of its resources (e.g. diversity, foraging strategy), two crucial factors in defining the ecological realized niche. In this study, we examine the ecological significance of newly defined isotopic functional indices, using a large set of associated species from two marine benthic communities widely reported in coastal shallow waters: the common brittle star Amphiura filiformis community competing with the crustacean amphipod Haploops nirae community.

We showed that Isotopic Functional Richness (a measure of the extent of the community trophic niche) is higher in the Haploops community due to a higher diversity in food sources but also due to longer food chains. Isotopic Functional Evenness (the regularity in all species distribution) showed that the biomass originates from other primary production sources, besides the phytoplankton.

These isotopic metrics responded according to expectations, based on the extensive knowledge of those communities. They provide new insights into how the structure of energy accumulation as biomass between species is likely to underpin the structure of the communities.

Image caption: Haploops nirae, a gregarious tubiculous amphipod (crustacean) species (top picture) colonizing muddy marine sediments and engineering a unique habitat (bottom picture) while largely affecting associated species assemblages.
You can read the full article here.

 

Convergence of three mangrove species towards freeze-tolerant phenotypes at an expanding range edge

Susan C. Cook-Patton, Michael Lehmann and John D. ParkerBranch samples collected from adult trees (photo credit: Susan Cook-Patton).

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Although many species are moving around as the climate changes, they are not all moving at the same rate. To help explain why three species of mangroves are migrating northwards at different rates, we examined variation in their ability to tolerate freezing temperatures. We sampled mangrove adults and seedlings along most of Florida’s eastern shoreline and exposed them to freezing temperatures. We also measured a suite of leaf and branch traits to examine how plants were changing as they grew closer to the range edge. We found that black mangroves, the most northerly and fastest migrating mangrove species, showed the greatest freeze tolerance, followed by red, and then white mangroves, the least northerly and most slowly migrating species. However, freeze tolerance as well as other traits were not fixed within species, but instead varied systematically with latitude. Adults from black and red mangroves showed higher freeze tolerance towards the range edge, and the leaves of all three species became denser, tougher, and smaller in the north than in the south. Thus, freeze tolerance appears to determine where mangrove species can move and at what rate. As freeze events become more and more uncommon, these species are likely to continuing moving northwards, but at different rates, possibly breaking apart plant communities that historically co-occurred.

Image caption: Branch samples collected from adult trees (photo credit: Susan Cook-Patton).
You can read the full article here.

 

Stress, hormones, and blood- the devil’s in the details

Jeffrey M. Goessling, Heather Kennedy, Mary T. Mendonça, and Alan E. WilsonA sample blood smear from an adult Gopher Tortoise (Gopherus polyphemus) with an elevated heterophil:lymphocyte ratio consistent with an acute stress response. Image credit: J.M. Goessling.

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Who hasn’t been stressed out? Although one could easily define what it feels like to be under stress, few could quantify their level of stress. So, what is stress? In the strict sense, it is a term to describe the physical pressure on a system from an outside source. For example, the weight of a floor resting on an I-beam. Historically, biologists have used the tools of endocrinology to measure stress on animal populations (that is to measure the degree to which the environment is exerting pressure on individuals). Specifically, hormones aptly referred to as “stress hormones” have been measured in individuals, and compared between “stressed” and “non-stressed” populations. However, while convenient, recent studies have indicated that stress hormones may not be reliable in indicating if animals are exposed to long-term stressors. One new approach to measuring stress is quantifying relationships among cells of the immune system, as it is well-known that stressors can elicit a change in how the immune system functions. In this paper, we quantitatively synthesized relevant literature (in a meta-analysis) to compare the traditional measure of stress (stress hormone concentration) to the more novel measure of stress (proportion of white blood cells) in studies that have been published using both methods. We found that both measures are in fact increased in populations exposed to stress. However, an important difference between the two measures is how individuals physiologically adapt to stressors over time. Specifically, elevated stress hormones are reduced in response to long-duration stressors, up to a point where they reach levels of non-stressed populations. This reduction in response to stress was not seen in the white blood cell counts. This suggests that the immune cell measure remains elevated in populations that have been exposed to stressors for a prolonged period. Therefore, conclusions from our study indicate that the white blood cell parameter could be very useful as a tool to test whether populations have been exposed to long-term stressors, while stress hormone concentrations should be interpreted cautiously as they may not be indicative of responses to long-term stress.

Image caption: A sample blood smear from an adult Gopher Tortoise (Gopherus polyphemus) with an elevated heterophil:lymphocyte ratio consistent with an acute stress response. Image credit: J.M. Goessling.
You can read the full article here.

 

Early life stages dictate the future: plant species sorting along water availability gradients

Rob G.A. Fraaije, Cajo J.F. ter Braak, Betty Verduyn, Leonieke B.S. Breeman, Jos T.A. Verhoeven and Merel B. Soons Ecologists at work.  Photo provided by authors.

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Plant species differ widely in their requirements and tolerances to environmental conditions. Though many studies are available on such requirements and tolerances, it often remains unclear at which stage of a plant’s life cycle such characteristics are mainly determined. Early stages in a plant’s life cycle are known to be sensitive to the environment, but several steps can be distinguished within the early stages, including seed germination, seedling survival, and seedling growth.

Stream ecosystems and their surrounding terrestrial areas, known as riparian zones, provide an example of highly diverse ecosystems, harbouring many different plant species that typically have individual preferences along a gradient from wet (in the stream) to moist (close to the stream) to dry conditions (further upland). This presents an ideal study system to test how early stages in a plant’s life cycle may contribute to a species preferred position along this gradient. We tested this by sowing seeds and planting seedlings of 17 riparian plant species across a riparian gradient from wet to dry conditions, while closely studying their responses afterwards.

The moisture gradient had a very strong effect on germination, seedling survival and seedling growth of all 17 plant species. All three processes were strongly inhibited at the wet and dry ends of the gradient. Moreover, the individual plant species showed their own specific preference along the gradient, especially during seed germination and seedling growth, corresponding to their preferred habitat as an adult plant. This showed that these early stages already set the template for vegetation patterns along streams, and that they contribute to a high biodiversity by separating species along moisture gradients. This is important knowledge given the major declines in riparian plant species diversity, and may help future conservation and restoration programs.

Image caption: Ecologists at work. Photo provided by authors.
You can read the full article here.

 

How does a winter desert annual cope with two challenges in the desert: summer rains and winter rain unpredictability

Alejandra Martínez-Berdeja Exequiel Ezcurra & Mauricio TorresRigid spineflower skeleton at the end of the growth season. Photo: Alejandra Martínez-Berdeja.

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The rigid spineflower (Chorizanthe rigida) is a winter desert annual that grows in the Mojave and Sonoran deserts. Most winter annuals disintegrate and disperse their seeds at the end of spring, but the dead spineflower plants form dry rigid skeletons that stay in the field for several years, releasing seeds in response to winter rain events. C. rigida’s unique dispersal mechanism seems to allow it to synchronize seed release with available soil moisture, a scarce and precious resource in deserts. However, in order to do so effectively, the plant needs to overcome two challenges. On the one hand, it has to be able to differentially respond to seasonal precipitation patterns and avoid germination after summer rains, when the scorching temperatures could kill them. On the other hand, the plants also face winter rainfall unpredictability in the desert: any single rain event that might cause seeds to germinate might or might not be followed by additional rainfall, putting germinated seeds at a risk of dying from dehydration.

Our study shows that the stalk that attaches the seeds to the plant in spineflowers is much thicker in bi-seasonal deserts with summer rains, allowing the plants to retain seeds beyond summer and release them to more favorable winter rainfall cues. Secondly, we found that seeds in C. rigida individuals from populations experiencing highly unpredictable winter rainfall are much more variable in size than those from more predictable desert sites. Subsequent germination trials showed that larger seeds need more water to germinate and therefore have lower short-term germination and display a more “cautious” germination strategy. Thus, highly variable seed sizes allow C. rigida individuals to exhibit a heterogeneous germination response in extreme deserts, thus avoiding the loss of large fractions of seeds after a false moisture cue. Our study shows how desert organisms can adapt to both rain seasonality and unpredictability through simple changes in reproductive morphology.

Image caption: Rigid spineflower skeleton at the end of the growth season. Photo: Alejandra Martínez-Berdeja.
You can read the full article here.

 

How Energy Allocation Influences Reproductive Success in the Southernmost Breeding Mammal, the Weddell seal

Michelle R. Shero, Riley T. Krotz, Daniel P. Costa, Julie P. Avery & Jennifer M. BurnsWeddell seal, photo provided by authors.

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The ability of animals to stay in good health despite drastically changing environmental conditions is important for individual survival and reproductive success. An animal that is in good health can catch enough food to maintain their own body mass, and gain weight in the form of fat (lipid) or lean tissue reserves. The allocation of ingested calories is regulated by a suite of hormones, such as cortisol, thyroid hormones, growth hormone, and insulin-like growth factor-1. In seals, both the condition of females at the end of their fasting period, and the amount of energy gained while at sea, may influence a female’s probability of producing a pup the next year, as females that are too skinny may not be able to start a pregnancy or carry a foetus to term.

Weddell seals (Leptonychotes weddellii) are the southernmost breeding mammal in the world, and they live and reproduce in an extreme and rapidly changing environment. During the austral summer, females give birth, nurse their pups, breed, and moult while also reducing foraging efforts. By contrast, during the winter and pregnancy, animals forage intensively. In this study, we assess whether females that end the moult in better health (larger, more lipid stores) are more likely to return with a pup the next year, and whether pregnant seals “prepare themselves” for the upcoming lactation period by gaining more fat during the winter than non-reproductive females. Surprisingly, our study showed that both reproductive and non-reproductive seals gained similar amounts of mass and lipid during winter foraging. However, pregnant Weddell seals gain less mass during gestation than other seal species, explaining why previous studies show they must forage during lactation. Post-moult females with higher thyroid hormone concentrations were more likely to produce a pup the next year. Similarly, decreasing level of cortisol (stress) and maintaining growth hormone across the winter was shown to correlate with higher pupping probabilities. This study suggests that multiple hormones involved with energy allocation may also be indicative of positive reproductive outcomes. Understanding physiological factors that influence the probability of reproduction is important for assessing the species’ vulnerability to changes in ecosystem structure.

Image caption: Weddell seal, photo provided by authors..
You can read the full article here.

 

Active prey mixing as an explanation for polyphagy in predatory arthropods

Renata Vieira Marques, Renato Almeida Sarmento, Felipe Lemos, Marçal Pedro-Neto, Maurice W. Sabelis, Madelaine Venzon, Angelo Pallini & Arne JanssenPicture provided by authors.

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The question of why some species specialize on one or a few food types, whereas others consume many, continues to puzzle scientists. The existence of both strategies suggests that there are advantages and disadvantages to being a specialist or a generalist. Advantages to consuming various foods are to enable balancing of nutrients in the diet or diluting toxins present in each food type. In either case, a mixed diet yields a better reproductive performance of the animal than a single diet. Indeed, for us humans this comes as no surprise as we fare better on a mixed, varied diet.

Although there are many studies on the effects of mixed diets in animals, only a few show that animals actively search for different food types to obtain a mixed diet. In most studies, the different foods are offered together, so that the animals have plenty of food in the same area and can obtain a mixed diet without any effort. In this paper, we show that two species of tiny predatory mites (adults smaller than 1 mm) perform better on a mixed diet of two prey species, herbivorous mites that are pests of a biodiesel plant (Jatropha curcas) in Brazil. We show that females of each of the two predator species produce twice as many eggs on a diet consisting of the two prey species than when feeding on either of the two prey separately.

Moreover, we also show that the predators actually actively search for a mixed diet. This was done in the laboratory by offering the predators each prey species on a separate leaf of their host plant and by connecting the two leaves using a plastic bridge. So in order to feed on a mixed diet, the predators needed to spend time and energy to cross the bridge. Indeed they did so when the two leaves contained different prey species and much less when both leaves contained the same prey species. So the predators do what is good for them albeit at a cost: they actively commute between the two prey patches so as to obtain a mixed diet, thereby maximizing their reproductive performance.

Image caption: Picture provided by authors.
You can read the full article here.

 

The genetics of plant-plant interactions

Etienne Baron, Julien Richirt, Romain Villoutreix, Laurent Amsellem and Fabrice RouxPhoto provided by authors.

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Plant-plant interactions like competition are ecological and evolutionary processes that deeply influence natural communities. Studying their underlying mechanisms may be a key to understanding the structure and functioning of plant communities, which may in turn help to predict the response of plant communities to global change. However, we are only beginning to understand the genetics of competition. Notably, the identity of the genes involved in plant competitive ability still deserves deeper investigation. This exciting challenge calls for a multidisciplinary approach at the frontier between evolutionary ecology and genomics.

In this study, we adopted an ecological genomics approach to test whether the genetics of competitive ability of a local population of the model annual plant Arabidopsis thaliana was dependent on the identity of the competitor species. In a common garden experiment, the response of 48 A. thaliana genotypes to competition was estimated by looking at a suite of nine plant traits (including a proxy of seed production) in six competitive environments: absence of competition, intraspecific competition and interspecific competition with four species frequently associated with A. thaliana in natural plant communities (i.e. Poa annua, Stellaria media, Trifolium repens and Veronica arvensis). In addition, the biomass of its corresponding competitor was estimated in order to quantify the competitive effect of A. thaliana.

We showed that variation in the identity of the competitor might promote maintenance of genetic variation of A. thaliana at the local population scale and species coexistence at the community scale. We also demonstrated that the optimal strategies of A. thaliana in response to competition depend on the identity of the competitor species. Finally, we found that the genomic regions associated with the response of A. thaliana to competition depend on the identity of the competitor. This genomic map allowed us to identify the candidate genes related to plant-plant interactions.

Image caption: Photo provided by authors.
You can read the full article here.

 

UV radiation causes darkening of the larval cuticle, at the expense of adult immune function

Sara Debecker, Ruben Sommaruga, Tim Maes and Robby StoksMale Azure Damselfly (Coenagrion puella). Photo credit: Robby Stoks.

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Many animals, just like humans, get a tan when exposed to the ultraviolet radiation (UV) in sunlight. This darkening of the skin or cuticle is a result of the accumulation of the molecule melanin, which absorbs the harmful UV radiation and protects the body from damage. In addition, melanin performs several other functions inside the body. In many invertebrates, for example, it is also an important component of the innate immune system, where it is used to encapsulate pathogens, such as bacteria and parasites, with the aim of neutralising them. This process is called “melanotic encapsulation”. The formation of melanin used for UV defence and for immune function relies on the same enzyme pathway and the same resources, which are taken up through the diet and therefore, their availability can be limited. Consequently, there might be a link, or even a trade-off, between the quantity of melanin used for UV defence and immune function. Furthermore, it has never been studied whether UV radiation can affect the immune system in an invertebrate. Additionally, in animals that have distinct larval and adult stages, such as insects and amphibians, little is known about the mechanisms by which stressors experienced in the larval stage affect the adult after metamorphosis.

In this study, we exposed larvae of the Azure Damselfly (Coenagrion puella) to UV radiation to evaluate whether UV affects the accumulation of melanin in the cuticle. After metamorphosis, we measured the strength of the immune system in adults as the melanotic encapsulation response. We found that larvae that were exposed to UV accumulated more melanin in their cuticle and metamorphosed later and at a smaller mass than animals reared without UV. After metamorphosis, they also had a reduced melanotic encapsulation response, constituting the first proof for UV affecting immune function in an invertebrate. Importantly, animals that accumulated more melanin in their cuticle as larvae had a more severely impaired immune function as adults, meaning melanin was traded off between its different functions. Therefore, we identified a new mechanism by which stressors experienced in the larval stage carry over to the adult stage.

Image caption: Male Azure Damselfly (Coenagrion puella). Photo credit: Robby Stoks.
You can read the full article here.

 

Intensity, not strategy is key for estimating trait values

C. E. Timothy Paine, Christopher Baraloto and Sandra DiazDr Claire Fortunel measures leaf toughness at Nouragues Biological Station, French Guiana.

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Functional traits are attributes of plants and animals that affect their rates of growth, survival and reproduction. They affect the responses of organisms to their environment, and also reflect the effects of the environment on organisms. For example, consider wood density, a commonly measured functional trait, which affects how stiff and strong an individual tree’s trunk is. If known for all trees in a forest, it also indicates how much carbon is stored within that forest. Thus, because of their myriad effects, functional traits are used to answer many questions about individual species and ecological communities. The challenge addressed in this paper is that, in species-rich ecosystems, it is very difficult to measure the functional traits of every species, as many of them are vanishingly rare. We report the optimal method for sampling trees to estimate the functional traits of diverse forests.

We began with nine hectares of tropical forest in French Guiana, in which eight functional traits had been measured on every tree. This gave us the true values of each trait in each plot. We then, using computer simulations, applied 12 different trait-sampling strategies. To take a few examples, some of the strategies emphasised very common species, others a range of sizes, and others particular clumps of individuals. Because we wanted to optimize the sampling of functional traits, we simulated applying the strategies over a range of intensities, from 1% of the individual trees up to 50% of them.

The take-home message is that the way to successfully estimate the distribution of trait values in a species-rich forest is through intense field sampling. In other words, the more trees you sample, the better your estimate of functional traits. Of less importance is the strategy applied. Increased sampling improved the performance of all strategies. Importantly, a commonly applied strategy, looking up trait values out of a database, yielded poor results, especially in estimating the variation in trait values within a forest. Our conclusion is that there is no substitute for extensive sampling to accurately characterize the distribution of functional trait values in species-rich forests.

Image caption: Dr Claire Fortunel measures leaf toughness at Nouragues Biological Station, French Guiana.
You can read the full article here.

 

Welcome neighbours: cooperative fish benefit from settling close to each other.

Arne Jungwirth, Dario Josi, Jonas Walker, Michael Taborsky  A group of Neolamprologus pulcher (to the left) getting ready to defend their territory against predators (two Lepidiolamprologus elongatus and a mastacembelid eel; to the right). During the experiments, predators were confined in a plastic tube to prevent fish from harming each other. Foto: A. Jungwirth.

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Many animals defend territories against each other, but still prefer to settle close to neighbours. This is difficult to understand, especially when neighbours frequently fight over shared borders, and when large aggregations attract many predators. These conditions are met in the African cichlid fish Princess of Lake Tanganyika (Neolamprologus pulcher). Groups of these fish cooperatively care for offspring, and fiercely defend their territories against neighbours, yet still prefer to settle close to other groups. This creates colonies of variable sizes that attract many predators, resulting in higher predator densities inside colonies than outside. Here we asked what potential benefits the fish might gain from seeking the proximity of competing neighbours. Using SCUBA diving in the natural habitat of these fish in Zambia, we presented groups with their main predator and measured the effort they invested in the defence of their territory. Defending against these predators is costly, involving expenditure of time and energy, and considerable risk. We found that groups settling close to neighbours reduced their attack effort against the presented predator. However, as close neighbours contributed heavily to predator defence, similar levels of anti-predator attacks ensued across the entire range of group densities. Apparently, these fish benefit from settling close to one another by communal anti-predator defence, which allows them to save time, energy, and risk when being attacked. Hence the Princess of Lake Tanganyika benefits from joining forces in defence against a mortal threat, which seems to outweigh the costs of fighting one another. Such effects may be widespread in animals breeding in colonies, where grouping is often costly while no obvious benefits seem to compensate for the observed harm. Even without coordinated behaviour, improved “safety in numbers” applies not only at the level of individuals, but also of groups.

Image caption: A group of Neolamprologus pulcher (to the left) getting ready to defend their territory against predators (two Lepidiolamprologus elongatus and a mastacembelid eel; to the right). During the experiments, predators were confined in a plastic tube to prevent fish from harming each other. Foto: A. Jungwirth.
You can read the article in full here.

 

Diverse forests make efficient use of canopy spaced by the authors

Tommaso Jucker, Olivier Bouriaud and David A. CoomesCarpinus betulus growing in the understorey of a mixed-species forest patch in Bialowieza (Poland). Photo provided by the authors.

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There is increasing evidence that mixed-species forests are more productive and cycle key nutrients more efficiently than species-poor ones, providing a strong argument for safeguarding the biodiversity of these ecosystems. Yet the ecological processes which drive this positive association between diversity and ecosystem function remain poorly understood. One idea which has recently been gaining traction is that mixed-species forests may be able to use canopy space more efficiently than monocultures, and that this in turn explains their greater ability to intercept light and sequester carbon.

There are two reasons why mixed forests might efficiently exploit canopy space. The first is that combining species which position their leaves in complementary height tiers can promote the development of a multi-layered canopy. The second possibility is that because of decreased competition for light among neighbours, trees in mixture develop larger crowns compared to their counterparts growing in monoculture. As part of a European-wide project (www.fundiveurope.eu) exploring the effects of biodiversity on ecosystem function in forests, we measured the crown dimensions of nearly 13000 trees and used these data to test whether trees in mixture packed their crowns more densely and efficiently than those in monoculture. We found that across a wide range of forest types and different combinations of species, diverse tree mixtures were able to partition aboveground space much more efficiently than species-poor ones. Interestingly, this occurred primarily as a result of individual trees expanding the size of their crowns when growing in mixture, and not because combining trees of different species resulted in multi-layered canopies. Our study shows that species mixing promotes the development of denser and more structurally complex forest canopies, and provides an explanation for why diverse forest ecosystems tend to be more productive and have faster rates of nutrient cycling.

Image caption: Carpinus betulus growing in the understorey of a mixed-species forest patch in Bialowieza (Poland). Photo provided by the authors.
You can read the article in full here.

 

Tree efficiency in resource use does not relate to tree ability to withstand drought

Jean-Marc Limousin, Enrico A. Yepez, Nate G. McDowell & William T. PockmanPlastic troughs that covered 45% of the plot area were used to exclude a fraction of the rainfall and simulate more intense drought in a piñon-juniper woodland of central New Mexico in the southwestern United States.

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Plants must acquire carbon, nutrients and water from the environment in order to grow and survive. An analogy exists between economics and plant functioning by which one can define resource use efficiency as the amount of carbon gained through photosynthesis per unit of water, nutrients and carbon spent or invested in the process. Opposing views exist, however, regarding the role of resource use efficiency in plant tolerance to water limitation. High water use efficiency may be seen as advantageous to withstand drought because it means that more carbon is acquired per unit water transpired. On the other hand, it may be seen as a conservative “water saving” strategy of drought sensitive species who cannot afford to spend water for a low carbon return and are thus less competitive when water is limited.

To examine how water use efficiency, nitrogen use efficiency and carbon use efficiency relate to drought tolerance we compared them between piñon pine and one-seed juniper in the southwestern United States. These two species are good models for the study because they differ markedly in drought tolerance and water use strategy. Piñon pine has exhibited extensive mortality over recent drought episodes, while co-occurring juniper has suffered much more limited mortality. We experimentally manipulated rainfall using plastic troughs that excluded a fraction of the precipitation in one plot, and sprinklers for irrigation in another plot. This resulted in three different drought intensities (partial rainfall exclusion, natural drought, and partial irrigation, from the driest to the wettest) for the two species in a common ecosystem.

Our results show that increasing water limitation increased water use efficiency in the two species. In other words, the trees maximize the efficiency of their use of the most limiting resource, i.e. water. This comes at the cost of lower nitrogen and carbon use efficiency as the water limitation of photosynthesis prevents the trees from making efficient use of their other resources. Differences were larger across treatments, in response to water limitation, than between the two species, which exhibited a convergence in resource use efficiency. We conclude that drought tolerance and survival in juniper is linked to its ability to keep performing photosynthesis under more intense drought, and not to a more or less efficient use of resources.

Image caption: Plastic troughs that covered 45% of the plot area were used to exclude a fraction of the rainfall and simulate more intense drought in a piñon-juniper woodland of central New Mexico in the southwestern United States.
You can read the article in full here.

 

Blossom colour change decreases the costs of reproduction

Christophe Pélabon, Lauriane Hennet, Richard Strimbeck, Hansen Johnson, William S. ArmbrusterDalechampia scandens blossom A) during the pollination period, and B) during seed maturation. C) Change in the colour of the bract over a period of approximately 10 days. (Photos C. Pélabon).

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Flowering plants invest significant amounts of energy in the development of flowers, seeds, and fruits. Structures such as petals and subfloral bracts are part of that energy cost and sometimes remain on the plant after they have served their primary function as pollinator attractants. This persistence may impose additional energy costs in the form of maintenance respiration or further developmental changes, which may include post-pollination colour changes. Consequently, it seems likely that these persistent structures may serve secondary functions during fruit and seed development. We addressed this question in a study of the neotropical vine Dalechampia scandens. In this species, male and female flowers are clustered in inflorescences (blossoms) that are subtended by two leaflike, showy bracts that are white during pollination, but turn green after closing around the developing fruits. The green bracts may conceal developing seeds from seed predators, but photosynthetic activity in the bracts could also provide a local source of carbon to the developing seeds. We tested this photosynthetic augmentation hypothesis by experimentally manipulating the bracts in hand-pollinated blossoms and comparing seed development among the treatments, and by measuring photosynthesis and dark respiration in blossoms with and without bracts, and before and after greening. When bracts were removed or their photosynthetic activity was prevented by shading, the blossoms produced smaller seeds than normal. Furthermore, the greening of the bracts sufficiently enhanced their photosynthetic activity to produce a positive energy balance for the whole blossom in the post-pollination period, that is, to at least partly offset the total cost of producing blossoms, fruits, and seeds. This energy benefit may explain why bract retention has appeared at least twice in the evolution of the Dalechampia genus, and is found in numerous species within the genus. Finally, this study illustrates how developmental and physiological flexibility can function in fine-tuning reproductive costs in the evolution of flowering plants.

Image caption: Dalechampia scandens blossom A) during the pollination period, and B) during seed maturation. C) Change in the colour of the bract over a period of approximately 10 days. (Photos C. Pélabon).
You can read the article in full here.

 

Root and leaf strategies synchronize in tropical montane forests in Borneo

Masayuki Ushio, Yasuto Fujiki, Amane Hidaka and Kanehiro KitayamaMt. Kinabalu from the southern slope of the mountain. This picture was taken from Park Headquarter of Kinabalu Park at about 1,560 m above sea level (©M. Ushio). One of our study sites (Intermediate P site) is a forest in the bottom part of the picture.

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Tropical forest trees in Borneo are gigantic, despite the fact that tropical soils contain small amounts of nutrients such as phosphorus (P), which are necessary to maintain and construct plant bodies. To maintain and construct such huge bodies, trees must have effective acquisition of soil nutrients as well as efficient use of the acquired nutrients.

In this study, we analyzed the ability of trees to degrade organic phosphorus, which needs to happen before it can be absorbed by roots, and morphological characteristics (such as surface area, diameter and tissue density) of the roots of the major tree species in three tropical montane forests on Mt. Kinabalu, Borneo. We also investigated the relationship between root and leaf properties. The amount of phosphorus in the soil in the three forests varies greatly from rich to intermediate to poor.

We found that the ability of roots to degrade organic phosphorus and root surface area increased while root diameter decreased with decreasing soil phosphorus. The results suggested that root properties change in a way that allows plants to effectively acquire phosphorus from soils. Furthermore, we compared root properties with leaf phosphorus concentrations of a given tree species. Interestingly, root phosphorus-degrading capacity increased with decreasing leaf phosphorus concentrations. This finding suggested that efficient phosphorus-acquisition of roots simultaneously occurs with conservative P use by leaves. There are several hypotheses to explain the results. Roots might detect low phosphorus concentration of leaves, and then could increase their ability to acquire phosphorus. Another hypothesis is that leaves with low phosphorus concentrations are shed beneath the tree crown, and roots must increase their ability to acquire phosphorus from such low phosphorus substrates. The truth is not known yet, but synchronized root and leaf strategies could be adaptive in phosphorus-poor tropical soils.

In conclusion, root nutrient-acquiring properties change along the gradient of soil phosphorus concentrations in the tropical montane forests, and the changes in root properties are coordinated with the changes in leaf P concentrations. Such synchronized root and leaf strategies could contribute to the maintenance/construction of tall forests on P-poor tropical soils in Borneo.

Image caption: Mt. Kinabalu from the southern slope of the mountain. This picture was taken from Park Headquarter of Kinabalu Park at about 1,560 m above sea level (©M. Ushio). One of our study sites (Intermediate P site) is a forest in the bottom part of the picture.
You can read the article in full here.

 

Basking sharks and oceanographic fronts: quantifying associations in the north-east Atlantic

Peter I. Miller, Kylie L. Scales, Simon N. Ingram, Emily J. Southall and David. W. SimsImage provided by authors.

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Basking sharks are the world’s second largest fish, and yet one of the most enigmatic species in the oceans. Relatively little is known about how they use their environment, and the ways in which they find sufficient foraging opportunities. As large marine vertebrates that feed exclusively on microscopic animal plankton, they require large volumes of food to survive. Basking shark populations in the north Atlantic are still recovering from the impacts of historical overexploitation, and remain threatened by increasing human pressure on the marine environment. A better understanding of their ecology is of great importance, both to our knowledge of how marine ecosystems work and for effective conservation.

Previous research has documented associations between basking sharks and ocean fronts – areas of the sea where two different water masses meet. Physical and biological processes that occur at fronts can lead to increases in plankton abundance, attracting marine predators such as the basking shark to forage at these features. However, the importance of these associations has not previously been established. Recent innovations in satellite remote sensing enable the detection and mapping of fronts in the surface ocean from space, and animal-mounted technologies can track the movements of sharks over timescales of weeks to months. This study combines these two technologies to investigate levels of association between basking sharks and ocean fronts in the north-east Atlantic.

Pop-off Archival Tracking (PAT) tags were used to track the movements of seven sharks during the regional surface sightings seasons (May – October) of 2001 and 2002. Satellite front mapping and statistical modelling reveal associations between these sharks and fronts in temperature and chlorophyll-a, a proxy for plant plankton abundance. Basking sharks appear to associate strongly with productive regions in which fronts develop frequently over the course of the summer, and with fronts that they encounter in real-time as they navigate their foraging seascape. Moreover, the persistence and strength of fronts appear to be important factors in their value as foraging features. These insights have clear implications for understanding the preferred habitats of basking sharks, and are useful in informing marine spatial planning and the management of human threats to populations in the region.

Image caption: Image provided by authors.
You can read the article in full here.

 

Trade-offs between trans-generational transfer of nutritional stress tolerance and immune priming.

Ikkei Shikano, Miranda C. Oak, Olivia Halpert-Scanderbeg & Jenny S. CoryHigh population density of cabbage looper larvae reduces food availability and increases risk of disease transmission (photo by Michael Hrabar).

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If parents experience a stressful environment it can sometimes have a strong positive impact on how their offspring fare in a similar environment, in essence, preparing them for what's to come. For example, in some animals, malnourished mothers can produce offspring that develop better under poor nutrient conditions. Similarly, mothers infected by a pathogen can transfer antibodies to eggs or fetuses to protect their offspring against that same pathogen. This capacity is not restricted to vertebrates, even invertebrates have shown this ability, which is particularly interesting since they do not have the ability to acquire immunity via antibodies.

However, providing for your offspring so that they are better equipped to survive can be energetically expensive for the parent. Therefore, we asked if parents are exposed to two sources of stress, in this case nutritional stress and a pathogen, would they equip the offspring for both stressors or would they select one over the other?

We tested this idea using the cabbage looper moth, Trichoplusia ni, by exposing parents to a pathogen (a bacterium) and poor food quality. These stressors are likely to occur together because as the population increases, food sources become depleted and the likelihood of coming into contact with an infected individual increases.

The results were intriguing. Parents that were exposed to the pathogen produced offspring that were highly resistant to that same pathogen. Similarly, parents that were given poor food produced offspring that developed faster on poor food, but interestingly these offspring were also highly resistant to two different pathogens, even though their parents never encountered them. This means that nutritional stress can also act as a cue for higher disease risk in the next generation. Our key finding was that when the parents experienced both stressors, they produced offspring that were resistant to pathogens but did not grow faster on a poor diet.

We have shown that experiencing multiple stressors can be important and could alter the response of a population to infectious disease.

Image caption: High population density of cabbage looper larvae reduces food availability and increases risk of disease transmission (photo by Michael Hrabar).
You can read the article in full here.

 

East West Home’s Best? Drivers of plant litter decomposition do not explain home-field advantage in subarctic tundra

Ciska G.F. Veen, Maja K. Sundqvist, David A. WardleField experiment in Abisko, Sweden. Photo credits: Ciska Veen.

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The decomposition of dead plant material, i.e. litter, is a crucial part of the recycling of carbon and nutrients in the soil. Decomposer organisms break down litter into organic and inorganic nutrients that can be taken up by plant roots and are used for plant growth. Recently, it became acknowledged that such decomposer organisms may be specialized to break down litter from plants in their vicinity (“home”) as compared to from other plants (“away”), referred to as “home-field advantage”. Although previous work has confirmed the existence of home-field advantage, it does not always occur. In our study, we aim to find out whether the quality of litter (e.g. nutrient content) and climate conditions can explain the strength of home-field effects.

Understanding what drives the strength of home-field advantage is relevant in the context of global change, where altered climate and associated changes in vegetation composition may decouple associations between plants and soil decomposer communities, which may influence key ecosystem processes such as decomposition and nutrient and carbon cycling.

To investigate our research question we set up a litter transplant experiment along a mountain slope in subarctic tundra in northern Sweden. We incubated different litter types in their “home” locations (i.e. where they originate from) and in other locations (i.e. with different litter qualities or different climate conditions). This allowed us to experimentally decouple litter types and environmental conditions, and hence to test how environmental conditions determine the breakdown of litter at home or away and hence the strength of home-field effects.

We found that the occurrence of home-field advantage in our study was limited and not related to litter quality or climate conditions. This indicates that the rate of decomposition was not affected by the experimental decoupling of litter and their own decomposer communities. Hence rapid shifts in plant community composition and temperature due to global change may not alter litter breakdown by decoupling plants from specialized decomposer communities in subarctic tundra.

Image caption: Field experiment in Abisko, Sweden. Photo credits: Ciska Veen.
You can read the article in full here.

 

Evolutionary conditions for floral colour change by plants.

Kazuharu Ohashi, Takashi T. Makino and Kentaro ArikawaVarious patterns of floral colour change. Photos by Kazuharu Ohashi (upper left, lower right) and Takashi Makino (upper right, lower left).

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Many of the 'adaptive' traits in animal-pollinated flowers occur in only some of the species within a taxonomic group. A typical example of such evolutionary pattern is floral colour change—the retention of old, non-reproductive, rewardless, but fully turgid flowers in an altered colour. This set of floral traits has been suggested as a plant’s strategy to enhance pollinator attraction from a distance while minimizing visits to non-reproductive flowers at close range. However, considering that most visually oriented pollinators would respond similarly to these aspects of floral display, the reason for the low prevalence of floral colour change in nature is unclear. /p>

We conducted a screening search for floral colour change in 219 flowering plants by quantifying the spectral alterations in petals while the flower is open and functional and translating the alterations into colour shifts through the eyes of insects. Using comparative methods that take account of shared evolutionary history, we further explored multiple possibilities that could account for the infrequent occurrence of floral colour change. An inspection of floral colour with UV-sensitive insect vision allowed us to identify more colour-changing species than previously noted. At the same time, many other species exhibited little or no colour change, even for insects. This interspecific variation in the degree of floral colour change was significantly explained by possible evolutionary benefits in interactions with bee pollinators, as well as constraints imposed by evolutionary history, biochemical aspects of pigments and functional requirements for post-changed colouration to maintain long-distance detectability while reducing close-range attractiveness. /p>

These results illustrate that an understanding of floral evolution requires the consideration of all possible causes of trait diversity in an integrative manner. In future, we plan to focus more closely on particular lineages and test the proposed hypothesis that floral colour change is a plant strategy to accommodate bees or comparable pollinators with memory-based spatial foraging, as well as the hypothesis that partial colour change in old flowers has evolved as a viable strategy to attract pollinators from a distance while deterring pollinators at close range.

Image caption: Various patterns of floral colour change. Photos by Kazuharu Ohashi (upper left, lower right) and Takashi Makino (upper right, lower left).
You can read the article in full here.

 

Revisiting old hypotheses on nitrogen, water and mimicry in mistletoes.

Marina C. Scalon & Ian J. WrightThe modified root (haustorium) of the mistletoe Muellerina eucalyptoides penetrating the bark of its host Eucalyptus hemastoma.

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Mistletoes are leafy parasitic plants, capable of photosynthesis, but completely dependent on their host plants for water and nutrients – which they “steal” by tapping into the vascular system (xylem) of host branches using a modified root (“haustorium”). Various hypotheses have been proposed to explain the characteristically high transpiration rates of mistletoes. The “N-parasitism hypothesis” posits that nitrogen is the key limiting nutrient for mistletoe metabolism thus fast transpiration is needed to obtain sufficient host N, and that low ‘water use efficiency’ (WUE) during photosynthesis is the result, particularly when parasitising hosts with low xylem N concentration. In a very different context, the "mimicry hypothesis" posits that, by having leaves that physically resemble those of their host, some mistletoe species (“mimics”) can deploy leaves with higher leaf N concentration than hosts yet avoid the higher vertebrate herbivory that would otherwise be expected. Although setting out to explain different phenomena the two hypotheses are linked via the focus on leaf N.

We tested these hypotheses at global scale using leaf N and δ13C data for 168 mistletoes-host pairs, from 39 sites sampled across all continents, except Antarctica (δ13C, the carbon isotopic signature, is an index of time-averaged WUE). We found no apparent link between mistletoe WUE and xylem N concentration in hosts (indexed via host leaf N concentration, or by whether or not hosts were N-fixers) and thus, no support for the N-parasitism hypothesis. However, the mimicry hypothesis was partially supported: mimic mistletoes showed higher leaf N concentrations than their hosts but, unexpectedly, only when growing on N-fixing hosts (presumed to invest heavily in N-based anti-herbivore defences; thus, this is a case of “Batesian” mimicry, i.e. one where a harmless species has evolved to imitate a harmful species).

Our findings suggest that N is not always the key limiting nutrient for mistletoes, or at least not the main nutrient driving faster transpiration. Further, we show for the first time that mistletoes – like their hosts – exhibit clear trait adaptations to environmental gradients. By reconsidering these issues at broad geographic scale and across a large number of species, our findings substantially modify current knowledge on the ecology and physiology of mistletoes and their hosts.

Image caption: The modified root (haustorium) of the mistletoe Muellerina eucalyptoides penetrating the bark of its host Eucalyptus hemastoma.
You can read the article in full here.

 

Plant identity drives biocontrol bacterial ability

Ellen Latz, Nico Eisenhauer, Stefan Scheu and Alexandre JoussetLolium perenne in a magenta box. Photo by Ellen Latz.

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Soil-borne plant pathogens represent a major threat to plant productivity. Breeding of resistant varieties is tedious and often inefficient, and current management strategies based on pesticide application have unknown side effects on the environment, soil fertility and human health. Interestingly, there are soil bacteria associated with plant roots that function as antagonists to plant pathogens by producing antibiotic compounds (biocontrol bacteria). However, factors controlling the production of antibiotic compounds are little understood. Plant specificity of biocontrol bacteria has been studied intensively, and bacterial effectiveness has been shown to be mediated by plant-induced shifts in rhizosphere (root-associated) microbial communities and plant-induced changes in the activity of biocontrol bacteria in producing antibiotic compounds. In grasslands primary production often increases with plant diversity and we hypothesised that, at least in part, this may be due to increased effectiveness of biocontrol bacteria in species rich plant communities. Unfortunately, information on plant-microbe interactions is based almost exclusively on plant monocultures, and little is known about plant identity effects in multi-species plant communities.

We investigated whether the activity of a root-associated bacterium in producing biocontrol compounds varies with plant identity in a plant diversity gradient. We set up a microcosm experiment with the model rhizosphere bacterium Pseudomonas protegens CHA0, an important biocontrol agent, and investigated effects of plant identity and diversity on the production of biocontrol compounds.

The expression of genes coding for biocontrol compounds was driven to a large extent by plant identity and persisted along the plant species richness gradient for all tested genes. Notably, the effect of plant identity varied between genes, indicating that plant species specifically impact bacterial gene expression.

Our results indicate that the presence of certain plant species in plant communities disproportionately impacts biocontrol traits expressed by rhizosphere bacteria, providing new insight into our understanding of the patterns driving plant health and productivity. We suggest that mixed cropping systems including certain key plant species may increase plant protection and thereby the sustainable management of agricultural systems.

Image caption: Lolium perenne in a magenta box. Photo by Ellen Latz.
You can read the article in full here.

 

A novel growth model evaluating Age-Size effect on long-term trends in tree growth.

Michinari Matsushita, Katsuhiko Takata, Gaku Hitsuma, Tsutomu Yagihashi, Mahoko Noguchi, Mitsue Shibata and Takashi MasakiJapanese Cedar plantation (photo provided by authors).

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To predict long-term changes in aboveground biomass and carbon stocks of forests accurately, it is essential to understand how intrinsic (e.g. size and age) and extrinsic (e.g. competition and resource status) factors affect tree growth. One of the major problems in understanding growth trends in long-lived trees is the difficulty of separately quantifying the effects of tree size and age. Because trees grow by accumulating tree rings, there is an axiomatic age-size correlation. Therefore, a tree growth model that can account for the complex growth-age and growth-size relationships is required to accurately identify long-term trends in tree growth, and to reliably predict forests’ responses to environmental changes. To address this issue, we develop a novel tree growth model. Our model assesses the trend in tree growth over time by explicitly partitioning the effects of age and size, while controlling for the covariation between them. The model is then extended to incorporate the effects of neighbourhood crowding and individual tree variation. To demonstrate our model, we apply it to long-term monitoring data from a mature (104-year- old) plantation of Japanese cedar. As a result, we observed a pronounced age-related decline in diameter growth. However, at each age, greater tree size was associated with higher growth rate. The growth-size curve predicted from the model became flatter with tree age, and the curve’s peak shifted rightwards as tree age increased. Although the relationships between growth, size and age in long-lived trees are very complex, we conclude that our growth model can reliably predict long-term trends in tree growth with respect to both age and size. In addition, the flexibility of our model will enable more robust testing of species-specific responses to long-term environmental changes.

Image caption: Japanese Cedar plantation (photo provided by authors).
You can read the article in full here.

 

Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis.

Rieta Gols, Roel Wagenaar, Erik H. Poelman, Marjolein Kruidhof, Joop J.A. van Loon & Jeffrey A. Harvey Cocoon of the solitary parasitoid wasp, Hyposoter ebeninus, (note the head capsule of the Pieris brassicae host caterpillar which is all that is left of the host). Bottom: cocoons (yellow) and the host caterpillar after egression of the gregarious (Cotesia glomerata) parasitoid wasps. (photo credits Tibor Bukovinszky, Bugs in the Picture ©. .

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Many plants produce volatile chemicals when attacked by herbivores. In the last two decades, many studies have investigated the role of these plant volatiles in attracting parasitoids and predators of herbivorous insects. The production of this attractive volatile ‘bouquet’ is often referred to as indirect defence strategy of the plant. However, the assumption that this enhanced attraction actually benefits the plant due to reduced herbivory has been rarely tested.

Parasitoids vary greatly in life-history traits that determine growth of their host following parasitism. For example, some parasitoids allow the host to grow while the parasitoid larvae develop inside of them, whereas others kill or paralyze the host immediately after parasitism. In addition, some parasitoid lay a single egg in a host (solitary life style) whereas others can lay broods of up to several hundred eggs per host (gregarious life style).

In this experiment we compared seed production and seed quality traits in a short-lived annual plant (Sinapis arvensis or charlock mustard) when free of herbivory, exposed to healthy unparasitized caterpillars or caterpillars that were parasitized either by a solitary (Hyposoter ebeninus) parasitoid or a gregarious one (Cotesia glomerata). Both parasitoid species allow the host, larvae of the large cabbage white butterfly, Pieris brassicae, to grow following parasitism, though not to the same extent, and both healthy and parasitized caterpillars feed on the foliage and the flowers of their food plant. We compared results obtained from experiments in the greenhouse and outdoors, as many researchers examining plant defences against insects conduct their experiments under controlled conditions in the greenhouse or laboratory.

Plants indeed benefitted from parasitism and the effects were slightly more pronounced when the caterpillars were parasitized by the solitary rather than by the gregarious wasp. This was caused by the greater reduction of feeding damage to the plant’s reproductive tissues by the former species. Results were only significant for the experiments conducted outdoors, illustrating the difficulties in relating experiments performed under controlled greenhouse conditions to more realistic field experiments.

Image caption: Cocoon of the solitary parasitoid wasp, Hyposoter ebeninus, (note the head capsule of the Pieris brassicae host caterpillar which is all that is left of the host). Bottom: cocoons (yellow) and the host caterpillar after egression of the gregarious (Cotesia glomerata) parasitoid wasps. (photo credits Tibor Bukovinszky, Bugs in the Picture ©. .
You can read the article in full here.

 

Vitamin E deficiency in last-laid eggs limits growth of yellow-legged gull chicks

Marco Parolini, Maria Romano,, Manuela Caprioli, Diego Rubolini & Nicola SainoYellow-legged gull chicks at hatching (photo credit to Marco Parolini).

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Mothers transfer to their eggs substances that have important effects on their offspring. However, in order to increase their reproductive success, mothers may favour particular eggs over others. For example, in birds the first eggs in a clutch are often of better quality than the eggs that are laid subsequently.

Vitamins are important components of the egg yolk where they accomplish crucial physiological functions. Vitamin E has a major role in protection against oxidative stress. Although the beneficial effects of physiological levels of vitamin E for organisms are well known, the consequences of variation in the concentration of vitamin E in the eggs are largely unknown.

In this study we tested if the injection of a physiological dose of vitamin E in the yolk has beneficial effects on growth of yellow-legged gull (Larus michahellis) embryos, resulting in larger body size at hatching. In gulls, the concentration of vitamin E declines with laying order of the three eggs which constitute the typical clutch, suggesting that mothers are limited in the amount of vitamin E they can allocate to the eggs and that they favour their first-laid eggs. For this reason, we expected that our experimental manipulation would enhance body size of chicks hatching from third eggs in particular.

Indeed, we found that chicks from vitamin E injected third-laid eggs were larger than chicks from control third-laid eggs, whereas chicks from first- and second-laid eggs did not benefit from vitamin E supplementation.

Yellow-legged gulls are known to adopt a so-called ‘brood reduction strategy’ whereby chicks from first- and second-laid eggs are favoured over those from third-laid eggs, which seldom survive. This strategy is thought to increase parental reproductive success by leading to larger investment in offspring which are most valuable from a parental perspective. Our results suggest that differential allocation of vitamin E to the eggs according to laying order is part of such parental favouritism strategy because it can contribute to a hierarchy of reproductive value among progeny members.

Image caption: Yellow-legged gull chicks at hatching (photo credit to Marco Parolini).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Conquering the world in leaps and bounds: hopping locomotion in toads is actually bounding

Stephen M. Reilly, Stephane J. Montuelle, Andre Schmidt, Emily Naylor, Michael E. Jorgensen, Lewis G. Halsey and Richard L. Essner, JrAn American toad (Anaxyrus americanus) in mid bound about to land on his feet and jump again without stopping.   Photo credit: Steve Reilly.

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Early frogs evolved jumping and simply crashed landed on their bodies. Later frogs mastered the ability to land on their arms and folded up legs so that they were ready to jump again. Jumping was perfected as an escape behavior that became the primary mode of locomotion in this prolific vertebrate group.

Most semiaquatic frogs are ambush predators, using one or two powerful jumps to escape their own predators, but other frogs have become terrestrial and use repeated shorter hops as their primary way of moving over land in search of food. Hopping frogs have traded long jumps for camouflaged toxic skin to discourage predators, can survive and breed in drier terrestrial habitats, and have greater endurance for sustained hopping on land. The toads are the most successful group of terrestrial frogs in terms of both diversity and geographic distribution. They diversified rapidly in the Oligocene (34 to 23 million years ago), expanding across nearly all continents. Even today, the cane toad continues to illustrate the terrestrial prowess of toads as they invade new areas in the Caribbean islands, Florida, the Philippines and Australia where humans have introduced them.

While many studies have revealed the numerous terrestrial adaptations of toads, their sequential hopping behavior, per se, had not been studied. When we compared the kinematics, forces and field occurrence of single hops and multiple hopping sequences in toads we discovered a novel aspect of locomotion adaptation that adds another facet to their exceptional terrestrial locomotor abilities.

We found that bouts of repeated hopping are not a sequence of normal hops but a series of bounding strides where toads land on their extended feet and jump again without stopping. In addition, free-ranging toads appear to use bounding locomotion more frequently than single hops. Bounding has the advantage of maintaining velocity and producing longer jump distances, while cyclic bounding steps reduce energy expenditure.

This is the first case of the common use of a bounding gait outside of mammals. Bounding adds a key terrestrial locomotor trait that helps explain toads’ history of global expansion and the challenges to modern faunas as introduced toads rapidly invade new ecosystems today.

Image caption: An American toad (Anaxyrus americanus) in mid bound about to land on his feet and jump again without stopping. Photo credit: Steve Reilly.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

An insecticide alters personality in jumping spiders.

Raphaël Royauté, Christopher M. Buddle & Charles VincentFemale Eris militaris. Image provided by authors.

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Insecticides are major stressors for many organisms, including beneficial organisms such as predators (e.g., spiders). Most insecticides degrade rapidly after spraying, but traces can persist in the environment. Insecticides often target the nervous system and, at low concentrations, act in a similar way as drugs do in humans. These sublethal doses are unlikely to kill exposed individuals but can affect behaviours such as locomotion, learning capacities and memory. Most studies on insecticides compare changes in average behaviour between exposed and non-exposed populations, but there is another layer of variation that is frequently overlooked: individual variation in behaviour. In any population some individuals are more active, more aggressive or consume more food. These “personality differences” are extremely common in nature and affect an individual’s fitness. The degree to which insecticides can affect personality differences is currently unknown. Our study aims at understanding whether insecticide exposure can alter personality differences in the Bronze Jumping Spider (Eris militaris), an important generalist predator in apple orchards.

We tested how a widely used organophosphate insecticide (phosmet) affected the amount of personality differences in two traits with important fitness consequences for spiders. We tested activity and prey capture behaviours before and after insecticide exposure for 95 individuals and compared those results to a control group of 81 spiders. We found no differences in average behaviour across treatments, but personality differences were reduced by 23% in the insecticide-treated group. We also noticed strong sex-specific variations in the way males and females coped with the insecticide. Males were most affected in the way they explored their environment but their capacity to capture prey remained intact. Females showed a decrease in the relation between activity and prey capture traits. Inactive females typically captured prey more quickly, which was not the case in the insecticide-exposed group.

These results are important because they suggest that scientists frequently underestimate the toxicity of insecticidal compounds by ignoring effects occurring at the individual level. In other words, individuals coming “under the influence” of insecticides typically no longer behave as their personality would predict. These personality alterations may affect a spider’s ability to efficiently suppress pests in agricultural settings.

Image caption: Female Eris militaris. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Stored grain pest parents protect offspring from bacterial infection in both laboratory and natural populations.

Ann T. Tate and Andrea L. Graham Gregarine protozoa infect the gut of a flat grain beetle collected from a feed mill. Photo credit: Ann Tate.

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Adult insects that are exposed to bacteria can produce offspring that are more likely to survive if they, in turn, become infected with the same bacteria. This phenomenon of enhanced survival is known as “trans-generational priming,” and has previously been demonstrated for a variety of insect species in laboratory settings. Trans-generational priming has sparked substantial interest for its potential application toward understanding and even manipulating the progression of infectious diseases in wild populations of insects, including vectors of human and livestock diseases and the biological control of agricultural pests.

However, it is unclear whether the lessons learned from laboratory experiments can be extrapolated into our predictions for wild populations, which are subject to higher levels of genetic and environmental variability. In this study, we perform experiments on flour beetles (Tribolium spp.) to demonstrate that trans-generational priming against the biological pest control candidate bacterium Bacillus thuringiensis (Bt) enhances post-infection survival and alters development rates of offspring in both a laboratory beetle colony and a wild population infesting a grain elevator. The parallels between laboratory and wild populations are accompanied by an important caveat, however: wild beetles that were infected with a common gut parasite were not able to bequeath the enhanced anti-bacterial protection to their offspring. Because these gut parasites occur frequently in species of stored grain pests and other agriculturally and economically important insects, accounting for co-infection by multiple parasites will be necessary for predicting the impact of trans-generational priming on disease dynamics in wild insect populations.

Image caption: Gregarine protozoa infect the gut of a flat grain beetle collected from a feed mill. Photo credit: Ann Tate.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

How to package information into feather color patches.

Alexis S. Chaine and Bruce E. Lyon A male lark bunting showing off his dapper plumage during the breeding season (Photo by Bruce Lyon).

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Many animals communicate with each other using color patches whose size or color can indicate the quality or health of the signaler. In animals with more that one color patch, a question is whether each patch communicates different information or whether patches work together to reinforce the same information. To answer this question, researchers often focus on how other individuals respond to the signals, but another approach is to study whether the different signals link together and how they change over time. We studied lark buntings —the Colorado state bird—across five breeding seasons to understand what information male plumage color patches could provide. Male lark buntings settle aggressive contests by comparing their relative plumage coloration and female lark buntings choose their mates based on the color and size of male color patches. In fact, females differ in what they like across years, and this attention to detail helps them produce more young. To investigate whether different plumage patches provide similar or different information, we looked at patterns of color variation among males and how the combination of color patches changes from one year to the next. Overall, we found that the size and color of most plumage patches were typically not linked to the value of other patches and likely provide different information. As a result, males had a mix of different quality patches. In addition, males regrow new feathers once a year and the size and color of different patches changed independently across years, an indication these different patches do not simply provide the same information to an onlooker. Nonetheless, most males came back with reasonably similar versions of each color patch, which tells us that some of the qualities advertised in plumage are inherent to the individual bird. Finally, the fact that some plumage patches show similar changes across most years suggests that these signals are influenced by large-scale environmental effects like climate. Overall, we showed that a longer term view of plumage signals can reveal a lot about what information these signals can communicate.

Image caption: A male lark bunting showing off his dapper plumage during the breeding season (Photo by Bruce Lyon).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Host-plant genetics determines the composition of associated insects.

Matthew A. Barbour, Mariano A. Rodriguez-Cabal, Elizabeth T. Wu, Riitta Julkunen-Tiitto, Carol E. Ritland, Allyson E. Miscampbell, Erik S. Jules, and Gregory M. CrutsingerInsect species associated with two different genotypes of coastal willow (Salix hookeriana).

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Just as people prefer different varieties of crops (e.g., Fuji vs. Red Delicious apples), insects prefer to feed on particular genetic varieties of the same plant species. Consequently, genetic variation within plants can result in different compositions of associated insect species. Surprisingly though, we don’t often know why these genetic varieties of the same plant species are attacked more by certain insects compared to others. Knowing why is critical for making predictions about how shifts in the genetic diversity of a plant population will have cascading effects on the species that rely upon them.

To figure out why, we conducted a detailed case study of 26 unique genetic varieties (genotypes) of coastal willow (Salix hookeriana), a dominant plant species that lives in coastal riparian and dune ecosystems of northern California. Specifically, we conducted surveys to identify insect species feeding on each willow genotype and how abundant each species was. We also screened the willows for 40 different traits that we suspected would influence how tasty they were (e.g., amount of toxins, nutrients, and water in leaves) and how much food and shelter they provided for the associated insects.

We often found that several traits were important in explaining the abundance of insects on the different willow genotypes, indicating that different insects might cue in on different aspects of the plants when choosing a host. In particular, there were more insects on larger plants, probably because they provided more food and shelter. We also found substantial variation among willow genotypes in the amount of toxins, nutrients, and water in their leaves. However, these traits were relatively less important than plant size, likely because many of the insects are specially adapted to feeding on willows and are able to tolerate variation in leaf chemistry. Despite measuring all of these traits, we still found that we were not able to fully explain why the composition of insect species varies with the genetics of their host-plant. This suggests that future research should consider other factors that may influence how an insect chooses a host-plant, perhaps including competition for food with other insects or avoiding being eaten.

Image caption: Insect species associated with two different genotypes of coastal willow (Salix hookeriana).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Red is the colour: the effect of trap colour and trap-flower distance on prey and pollinator capture in carnivorous sundews.

Andreas Jürgens, Taina Witt, Amber Sciligo, Ashraf M. El-Sayed Two sundew species with red prey-trapping leaves:  Drosera arcturi (top), Drosera spatulata (bottom). Photos: Andreas Jürgens.

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Carnivorous plants feed on insects as an adaptation to nutrient poor soil conditions. Thus, the features of the prey-trapping leaves of carnivorous plants are very likely under strong selection pressure to optimize prey capture. The functional features of carnivorous plants’ traps such as colour of the trap leaves have been mostly interpreted as adaptations to capture prey. However, carnivorous plants that feed on insects run the risk that insects that are needed for pollination also land on the traps. Such a feeding habit may have negative effects on pollen import and export and in consequence on plant reproductive success. It is therefore assumed that the so called pollinator-prey conflict in carnivorous plants might play an important role in the evolution of trap features. In carnivorous plants with sticky leaves, such as Drosera and Pinguicula, the spatial distance between traps and flowers and also the colour of the traps likely play a role in attracting prey but they may also affect the risk of potential pollinators landing on a trap. It has been reported that red pigmentation in carnivorous plants may lure insect prey to traps. Indeed many carnivorous plants turn red when they are “hungry” (low in macronutrients). If this is the case the red colour of carnivorous plants can be interpreted as a way to attract more prey. However, this idea remains controversial because colour vision in most insects does not extend very far into the red part of the spectrum. For most insects it is difficult to distinguish red from green.

We tested an alternative hypothesis, namely that red pigmentation of the trapping leaves may reduce the risk of a pollinator-prey conflict. Experiments were conducted in a natural habitat of two sundew species (Drosera arcturi and D. spatulata) in the Southern Alps of New Zealand. Using model flowers and sticky model traps similar in shape to Drosera leaf traps, we investigated the effect of colour (green vs. red vs. white), and flower-trap distance (flower stalk length and leaf arrangement i.e. upright as in D. arcturi vs. flat ground rosette as in D. spatulata) on composition and abundance of insects landing and being trapped.

We found that flower-trap distance had no significant effect on the risk of pollinators being trapped. Model flowers higher above the ground received more pollinator landings probably because they can be better seen in the vegetation. Across all model traps the number of trapped pollinators was significantly lower in traps with red leaves compared to green ones.

Our results suggest that the typical red pigmentation of the trapping leaves in Drosera may be a way to protect pollinators from being attracted and captured. However, pollinator protection via red traps may come with a trade-off because total prey capture was significantly lower in plants with red leaves.

Image caption: Two sundew species with red prey-trapping leaves: Drosera arcturi (top), Drosera spatulata (bottom). Photos: Andreas Jürgens.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Behaviorally escaping the heat of climate change may lead to long term vulnerability.

Lauren B. Buckley, Joseph C. Ehrenberger, and Michael J. Angilletta Jr.Joe Ehrenberger making physiological measurements on a Sceloporus lizard.

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Moving through landscapes to select microclimates to regulate body temperatures is viewed as central for mobile organisms to escape the heat as climate warms. However, behaviorally avoiding the heat may reduce selection for heat tolerance. This could hypothetically reduce variation in thermal tolerance across the distribution of a widespread species. We used a model of optimal thermal physiology to demonstrate the potential for this outcome, known as the Bogert Effect, for fence lizards in the Sceloporus undulatus species complex. We provide the most thorough test of the Bogert Effect to date using physiological data for populations across the North American distribution of this lizard. Empirical data for seven populations demonstrate similar thermal tolerance among populations, consistent with the model's prediction in the case of effective behavioral thermoregulation. In an eighth population, from a region where behavioral thermoregulation should be less effective, we observed greater heat tolerance and poorer cold tolerance, as predicted by our model. We next examined the consequences of the Bogert Effect for long term vulnerability to climate change. Our model indicates that lizards can avoid heat stress through behavioral thermoregulation in the coming decades. But animals must devote energy to behavioral thermoregulation, reducing the time available for foraging and exposing themselves to predators when seeking sun or shade. The potential to behaviorally compensate for climate warming may decline rapidly, forcing organisms to rely on physiological adaptation. However, rates of adaptation may be too slow for the organisms to respond to climate warming once behavioral thermoregulation becomes ineffective. Our analyses bolster concerns that behavioral buffering, while beneficial in the short term, ultimately limits the physiological adaptation required to endure a warming climate in the long term.

Image caption: Joe Ehrenberger making physiological measurements on a Sceloporus lizard.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits.

Staffan Jacob, Nathalie Parthuisot, Armelle Vallat, Felipe Ramon-Portugal, Fabrice Helfenstein & Philipp HeebGreat tit (Parus major). Image copyright Joris Bertrand.

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Microorganisms constitute the major part of the earth’s biomass and are remarkable in their diversity and ubiquity. Pathogenic microbes can modify their host’s allocation of resources, increasing the amount of resources allocated to protection at the expense of other fundamental tasks such as development and reproduction. In contrast, many beneficial microorganisms are essential for host digestion or nutrient synthesis. The host microbiome, defined as the whole community of microorganisms in contact with an organism, is thus expected to play a major role in species evolution, although experimental studies from natural systems are still lacking. Here we test whether the microbiome affects host reproduction in wild breeding Great tits Men(Parus major) by experimentally modifying their microbiome, by spraying the nests with liquid solutions that either promoted or inhibited the growth of bacteria. We show that the microbiome affects three important components of bird reproduction. First, if bacterial growth was inhibited, females reduced the amount of carotenoids deposited in eggs, a molecule with important anti-oxidant and immune-stimulant properties for nestlings. Second, nestlings grow faster and are bigger at fledging when exposed to lower bacterial densities. Finally, while reproduction is a costly activity that usually results in the excessive production of free radicals and therefore oxidative damage to the body, we show that modifying the bird’s microbiome can alleviate this oxidative cost of reproduction. Our study provides experimental evidence for a role of the microbiome in bird reproduction, demonstrating the major effect that the microbiome may have on the evolution of reproductive strategies and life-history traits.

Image caption: Great tit (Parus major). Image copyright Joris Bertrand.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The whitefly-associated facultative symbiont suppresses induced plant defenses.

Qi Su, Kerry M. Oliver, Wen Xie, Qingjun Wu, Shaoli Wang, Youjun ZhangWhiteflies feeding on tomato stems. Photo provided by authors.

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Herbivorous insects and plants have engaged in antagonistic coevolution for hundreds of millions of years. This process has led to the evolution of novel defenses in plants and counter-measures in insects, and fueled the diversification of both species-rich groups. Plants deploy a range of tactics to contend with insect herbivory, including the synthesis of toxic and repellant chemistry. Herbivores, in turn, have countered with diverse responses, including the detoxification and sequestration of defensive plant chemicals. Chemical defenses against herbivores are typically orchestrated by the jasmonic acid (JA) signaling pathway, which often acts antagonistically with the salicylic-acid (SA) pathway triggered by microbial threats. Emerging evidence indicates that another tactic in the arsenal of insects that eat plants is the modulation of plant signaling pathways to curtail plant defenses.

Insect herbivores are also frequently infected with maternally-transmitted bacterial symbionts, which are increasingly recognized to influence important ecological interactions. Here we demonstrate that the heritable bacterium, Hamiltonella defensa, infecting the whitefly Bemisia tabaci MED, suppresses induced defenses in tomato, Solanum lycopersicum to the benefit of the herbivore. We show that feeding by H. defensa-infected whiteflies inhibits the induction of JA and JA-related defenses, and that suppression depends on the SA signaling pathway. We also found that saliva applications collected from H. defensa-infected whiteflies suppressed induced defenses, suggesting that salivary factors present only in symbiont-infected whiteflies were responsible. This finding represents a novel role for arthropod heritable symbionts and yet another means by which insects can counter plant defenses against herbivory.

Image caption: Whiteflies feeding on tomato stems. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Biocrust-forming lichens effects on soil nutrients and microbial abundances.

Manuel Delgado-Baquerizo, Antonio Gallardo, Felisa Covelo, Ana Prado-Comesaña, Victoria Ochoa & Fernando T. MaestreClose-up view of the lichens dominating biological soil crusts at the Aranjuez Experimental Station: Diploschistes diacapsis, Fulgensia subbracteata and Psora decipiens (white, yellow and pink thalli, respectively). Photograph by Fernando T. Maestre.

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There is a lack of knowledge on how particular species of biocrust constituents (e.g. soil lichens) affect microbial communities and nutrient availability in the underlying soil.

Here, we evaluated the effects of six biocrust-forming lichens (Buellia epipolia, Diploschistes diacapsis, Fulgensia subbracteata, Psora decipiens, Squamarina cartilaginea Squamarina lentigera) on microbial abundance and multiple variables associated with soil nitrogen (N), carbon (C) and phosphorus (P) cycling. We also evaluated whether the composition of lichen tissues (contents in C, N, P and polyphenols) is related to C, N, P availability and microbial abundance in soils.

We found strong species-specific effects of the lichens studied on C, N and P availability in soil, and on soil microbial abundance. Inorganic P and amino acids were the most important factors differentiating lichen microsites. These effects seem to be related to the C, N and P composition of the lichen tissues. For example, soils under D. diacapsis and P. decipiens, which had the lowest and highest C, N and P contents in their tissues, respectively, had the lowest and highest nutrient availability, respectively. We also found lichen species-specific effects on soil microbes. For instance, F. subbracteata and D. diacapsis were negatively related to the abundance of bacteria compared to bare ground areas.

Our results support the idea that, as found with vascular plants, biocrust-forming lichens have species-specific effects on soil microbial communities and C, N and P cycling. Thus, continuing to consider biocrusts as a single entity will only add confusion to our knowledge of how they control nutrient availability and microbial abundance in the ecosystems where this key community is prevalent.

Image caption: Close-up view of the lichens dominating biological soil crusts at the Aranjuez Experimental Station: Diploschistes diacapsis, Fulgensia subbracteata and Psora decipiens(white, yellow and pink thalli, respectively). Photograph by Fernando T. Maestre. For additional BSC pictures from Aranjuez click here.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Highway to the danger zone: costs of immune system activation in an invasive lizard.

Amber J. Brace, Sam Sheikali& Lynn B. Martin Angry brown anole.

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In any natural environment, organisms will become hosts to many different types of parasites, including bacteria. Once exposed, the immune system of hosts activates to eliminate the parasite. However, this important host protection process is energetically expensive because it is often accompanied by an increase in metabolism and fever. In many populations, immune system activation results in decreased growth, reproductive success and other important processes, likely as an effect of the energetic costs mentioned above. These costs experienced by hosts vary greatly from population to population, and even individual to individual, and are likely partially responsible for the enormous variation that can be seen in how hosts respond to infection.

Many factors, including time of year (breeding or non-breeding season), food availability and ambient temperature can affect the costs incurred by hosts when their immune system is activated. Several studies have shown that the number of parasites an individual is exposed to and/or the number of times an individual is exposed can influence how hosts respond to infection, meaning that these factors play a large role in the costs experienced by exposed hosts. However, how host exposure influences costs of immune activation remains relatively unknown. In this study, we investigated whether exposure to increasing concentrations of an immune-activating component of Salmonella bacteria caused increases in host cost in an invasive lizard in Florida, the brown anole. This species is of ecological concern in Florida because it is very abundant, but little is known about how it may be affecting the spread of parasites. We found that this species of lizard does experience an increase in cost of immune activation with increased exposure to Salmonella bacterial components, but that these costs are quite modest. These findings suggest that because costs associated with infection in this species are low, they may not respond strongly to infection. If this is the case, brown anoles may be more likely to harbor high loads of Salmonella bacteria, which they will subsequently shed into the environment, increasing the probability of exposure in native reptiles.

Image caption: Angry brown anole.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The whitefly-associated facultative symbiont suppresses induced plant defenses.

Qi Su, Kerry M. Oliver, Wen Xie, Qingjun Wu, Shaoli Wang, Youjun ZhangWhiteflies feeding on tomato stems. Photo provided by authors.

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Herbivorous insects and plants have engaged in antagonistic coevolution for hundreds of millions of years. This process has led to the evolution of novel defenses in plants and counter-measures in insects, and fueled the diversification of both species-rich groups. Plants deploy a range of tactics to contend with insect herbivory, including the synthesis of toxic and repellant chemistry. Herbivores, in turn, have countered with diverse responses, including the detoxification and sequestration of defensive plant chemicals. Chemical defenses against herbivores are typically orchestrated by the jasmonic acid (JA) signaling pathway, which often acts antagonistically with the salicylic-acid (SA) pathway triggered by microbial threats. Emerging evidence indicates that another tactic in the arsenal of insects that eat plants is the modulation of plant signaling pathways to curtail plant defenses.

Insect herbivores are also frequently infected with maternally-transmitted bacterial symbionts, which are increasingly recognized to influence important ecological interactions. Here we demonstrate that the heritable bacterium, Hamiltonella defensa, infecting the whitefly Bemisia tabaci MED, suppresses induced defenses in tomato, Solanum lycopersicum to the benefit of the herbivore. We show that feeding by H. defensa-infected whiteflies inhibits the induction of JA and JA-related defenses, and that suppression depends on the SA signaling pathway. We also found that saliva applications collected from H. defensa-infected whiteflies suppressed induced defenses, suggesting that salivary factors present only in symbiont-infected whiteflies were responsible. This finding represents a novel role for arthropod heritable symbionts and yet another means by which insects can counter plant defenses against herbivory.

Image caption: Whiteflies feeding on tomato stems. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Sustained heat waves may reduce output of a parasite that causes frog deformities.

Sara H. Paull,Thomas R. Raffel, Bryan E. LaFonte and Pieter T. J. JohnsonInfected snail surrounded by a cloud of cercariae.

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Climate change is altering the size and frequency of temperature fluctuations, yet researchers are only beginning to test how shifts in temperature influence species interactions, including parasitism. A sudden shift in temperature can lead to reduced performance of an organism across a variety of basic functions (e.g., reproductive output, immune defenses). As the organism acclimates to a temperature change over time, its performance can sometimes improve, a process known as ‘beneficial acclimation’. If the new temperature is stressful, however, performance might instead be reduced. We studied how all combinations of temperature shifts from one of 5 initial temperatures (13, 16, 19, 22, 25°C) to one of 5 new temperatures (16, 19, 22, 25, 28°C) influenced the release of the parasitic flatworm Ribeiroia ondatrae from its snail host. We found that parasite release was highest at warmer temperatures shortly after the temperature shift, but parasite release became reduced following periods of more than 48 hours above 25°C. These results are contrary to the beneficial acclimation hypothesis and suggest that temperatures above 25°C are energetically stressful, causing reduced parasite performance following sustained exposure to warmer temperatures. Our results also suggest that infective stages might be stored within snails at lower temperatures for later release when temperatures warm. Ribeiroia’s next hosts are frogs, and the parasite can cause mortality and severe limb deformities in these amphibians, so these results have implications for frog conservation. Exposure of frogs to this deformity-inducing parasite might rise following a sudden temperature increase, or decrease following periods of sustained warm temperatures. Our results also provide insights into potential effects of climate on related trematode parasites of humans like schistosomiasis.

Image caption: Infected snail surrounded by a cloud of cercariae.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Personality, plasticity, and predation: linking endocrine and behavioural reaction norms in stickleback fish.

Ines Fürtbauer, Alice Pond, Michael Heistermann & Andrew KingThree-spined stickleback (Gasterosteus aculeatus) and robotic heron. Photographs by Ines Fürtbauer.

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How do animals respond to changes in their environment? Are certain individuals better able to cope with a potential threat? With increasing human activity all over the world, animals have to deal with many more and many different changes happening very quickly. Understanding how animals adapt to such changes is therefore a major and outstanding question for biologists.

Generally, individuals respond to a potential threat with an increase in stress hormone levels – a ‘physiological stress response’ which can mediate the way that individuals behave under threat – the ‘behavioural response’. Across the animal kingdom, individuals of the same species have been shown to consistently vary in their physiological and behavioural responses – they show “personality”. But does personality constrain “plasticity”? In other words, do certain personality types show a reduced capacity to respond to environmental change? This study set out to address this question by investigating the behavioural and physiological responses of three-spined stickleback fish to changes in perceived predation risk.

Across five weeks, we repeatedly exposed female fish to two different perceived predation pressures (low and high) using a robot bird that resembled a heron, a natural predator of the sticklebacks. We collected hormones excreted into the surrounding water via the fishes’ gills, and filmed the fishes’ behaviour. This allowed us to investigate whether individuals show personality, whether and how they hormonally and behaviourally respond to changes in predation risk, whether they are constrained in their response, and whether hormonal and behavioural responses are linked.

The fish showed consistent behavioural and hormonal responses and were less active, shyer, and showed increased stress hormone (i.e. cortisol) levels after exposure to the robot predator. Furthermore, individuals were shyer on days they had higher basal cortisol levels, indicating a link between hormones and behaviour. We found no evidence for variation between animals in their plasticity, suggesting that individuals are not constrained by their personalities in their response to changes in predation pressure. In other words, different personalities are equally capable of responding to a potentially harmful threat. Our study offers novel insight into the interplay of consistent individual differences in hormones and behaviour, as well as plasticity in response to environmental change.

Image caption: Three-spined stickleback (Gasterosteus aculeatus) and robotic heron. Photographs by Ines Fürtbauer.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plant aroma drives diversification of plant-herbivore-carnivore interactions.

Kinuyo Yoneya & Takeshi MikiLady beetles (Aiolocaria hexaspilota) search for leaf beetles (Plagiodera versicolora) using willow volatiles.

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Plants enhance the production of chemical toxins and physical barriers when attacked by herbivores (direct resistance). Many plants have also evolved another strategy, crying for help through emitting a special blend of aroma, which might effectively attract bodyguard carnivores that exclude herbivores (indirect resistance).

A blend of aroma transfers information useful to carnivores, such as herbivore species identity and damage levels. However, due to its diffusivity, the information is inevitably leaked and exploited by the herbivores. Thus plant aroma affects not only carnivore but also herbivore behaviour, involving them in an 'information war'. Herbivores face a dilemma of choice between intact and damaged plants, and have to balance plant quality and apparency (how easily the plant is found) with predation risk. Carnivores face a dilemma of choice between lightly- and heavily-damaged plants, and have to consider plant apparency and herbivore quality.

In order to predict the consequences of this information war, we have developed a simple food chain model of plant-herbivore-carnivore.

Our model clearly demonstrated that levels of direct resistance and the amount of plant aroma were key determinants of herbivore and carnivore behavioural responses to plant aroma, as the consequences of co-evolution. Under a wide range of conditions, the model predicts that carnivores should choose the plant aroma from damaged plants, independently of damage levels. The model also predicts that herbivores should choose (or avoid) the aroma from damaged plants when the level of aroma emission is low (or high). These two results imply that the plant aroma is highly likely to function as an effective form of indirect resistance, repelling pest herbivores and/or attracting bodyguard carnivores. Intriguingly, when direct resistance level is too high, the plant aroma from damaged plants attracts herbivore but repels carnivores. These results also explained the roles of plant aroma in several contrasting plant systems, including willow trees, Lima bean, and wild tobacco.

Our new findings will advance our understanding of plant resistances as a driving force of evolutionary diversification of animal foraging behaviour and thus complexity in ecological network structure.

Image caption: Lady beetles (Aiolocaria hexaspilota) search for leaf beetles (Plagiodera versicolora) using willow volatiles.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Prey density and distribution drive the three-dimensional foraging strategies of the largest filter feeder.

Jeremy A. Goldbogen, Elliott L. Hazen, Ari S. Friedlaender, John Calambokidis, Stacy L. DeRuiter, Alison K. Stimpert, and Brandon L. SouthallPhoto by Ari Friedlaender under NMFS Permit: #14534-2.

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Predators use a suite of foraging strategies to maximize their energetic gain and support their metabolism. Foraging in aquatic vertebrates can be broadly categorized into particulate feeding, where single prey items are seized and ingested, and bulk-filter feeding that involves the capture and processing of large volumes of prey-laden water. Several animal groups have independently evolved a bulk-filter feeding strategy, including cartilaginous fish (e.g. whale sharks and basking sharks) and baleen whales. Many filter feeders exhibit a ram-feeding mode where animals use their forward locomotion to drive water into the mouth where filtration occurs.

Large bulk filter feeders have long been assumed to be indiscriminate "vacuums" of the ocean, slowly filtering water regardless of variation in prey distribution, but here we reveal tremendous plasticity of foraging strategies in the world's largest filter feeder, the blue whale (Balaenoptera musculus), which is strongly a function of prey density and depth. Blue whales exhibit a unique mode of ram feeding called lunge feeding which involves the intermittent engulfment of large volumes of prey-laden water that are commensurate with the whale’s body size. Lunge feeding is a high-drag, high intake filter feeding strategy that requires high prey density for energetically efficient foraging.

We simultaneously measured whale foraging behavior and the characteristics of their sole prey resource, krill. Our analyses found that blue whales exhibit much more acrobatic lunge feeding events when foraging on small, low-density, more patchily distributed krill. In contrast, when foraging on dense, deeper, and larger krill aggregations, blue whales increased lunge frequency and maneuvered less during each lunge. These data demonstrate a previously unrecognized range of adaptable foraging strategies in a large bulk-filter feeder. Because maneuvering and diving require significant amounts of energy, the variation in foraging behavior that we revealed has major implications for optimal foraging and bioenergetic models.

Image caption: Photo by Ari Friedlaender under NMFS Permit: #14534-2.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Links between metabolic rates and growth depend on food availability.

Sonya K. Auer, Karine Salin, Agata M. Rudolf, Graeme J. Anderson, and Neil B. MetcalfePhoto of brown trout. Copyright Sonya Auer.

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Metabolic rates determine the energetic cost of living and can differ dramatically between individuals. At the very minimum is an individual’s standard (or resting) metabolic rate (SMR) – the energy it must expend on the maintenance of tissues and bodily functions needed to sustain life. Metabolic rates are thought to have important impacts on fitness, but results thus far are equivocal. Some studies find a negative while others find a positive correlation between SMR and different measures of fitness such as growth and survival. These inconsistencies might arise because links between metabolism and fitness depend on environmental conditions. Consideration of an individual’s aerobic scope (AS), in addition to its SMR, might also improve our understanding of the links between energy metabolism and fitness. Aerobic scope (the difference between SMR and maximal metabolic rate – after exhaustive exercise) determines the extent to which an individual can increase its metabolic rate above SMR to finance key functions such as digestion, locomotion, growth and reproduction.

We examined the links between individual variation in both SMR and AS and growth rates of brown trout (Salmo trutta) under different levels of food availability. We measured the SMR and AS of 120 juvenile trout and then fed each fish either a low, intermediate, or unlimited food ration in individual tanks in the laboratory. After two weeks we measured how much they had grown and examined whether the growth rates of individuals differing in their SMR and AS depended on food level. We found that an individual’s SMR was not correlated with its AS but both metabolic traits affected growth. However, their effects depended on each other and also on food level. Growth was faster at higher food levels, but individuals with different SMR and AS performed differently at each food level such that there was no combination of SMR and AS that was associated with the fastest or slowest growth at all food levels. These results demonstrate the importance of AS in explaining growth rates and provide evidence that links between individual variation in metabolism and fitness can depend on environmental conditions, in this case food level.

Image caption: Photo of brown trout. Copyright Sonya Auer.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

A cross-seasonal perspective on local adaptation: Metabolic plasticity mediates responses to winter in a thermal-generalist moth

Caroline M. Williams, Wesley D. Chick & Brent J. SinclairImage provided by authors.

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Across latitudinal and altitudinal gradients, environmental conditions vary strongly. To cope with these changing conditions, populations of organisms may be adapted to their local conditions, allowing them to survive and thrive better in their home environment than would populations from other regions. In temperate regions, this local adaptation must serve the organisms across their whole lifecycle, but characteristics that enhance survival and performance in one season may be detrimental in other seasons. Thus, to understand local adaptation we need to look at survival and performance across seasons, but most studies to date have focused only on the summer growing season. We tested for local adaptation to winter conditions in a common species of moth, Hyphantria cunea, which occurs throughout North America in diverse thermal environments. We collected larvae from the northern edge and centre of their geographic range, exposed them to both northern and central winter conditions in the lab, and monitored their survival and performance throughout the winter and into the next spring. We found that indeed the populations were locally adapted to their winter environment, with higher rates of survival and larger size and carbohydrate reserves when overwintered at their home conditions. This suggests that climate change may disrupt populations of this moth from their optimal conditions, and that populations may suffer if winter and growing season temperatures become decoupled.

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This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Changing drivers of species dominance during tropical forest succession.

Madelon Lohbeck, Lourens Poorter, Miguel Martínez-Ramos, Jorge Rodriguez-Velázquez, Michiel van Breugel & Frans BongersThe study area in Chiapas, Mexico, where the landscape consists of a mosaic of agricultural fields, young secondary forest and old secondary forest.

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Tropical forests are celebrated for their high aboveground biomass and high tree diversity. Here we study secondary succession: the process of forest recovery after complete clearance of the vegetation for agriculture. This represents a natural gradient of biomass and diversity build-up. As the forest grows back over time, some of the species that are present in the forest manage to attain high biomass and become dominant, whereas other tree species remain rare. We ask whether such dominance is related to the characteristics of the species (functional traits) and what mechanisms drive species dominance. Is it environmental filtering, i.e. does the environment select for specific types of trees? Or is it limiting similarity, i.e. successful species tend to be specialists that differ from other dominants?. We answer these questions by studying tropical secondary forest in Chiapas, Mexico.

We found that in young forests with low overall biomass the trees that are dominant, even if they are from different species, all have similar light capture strategies. Thus at this stage the main mechanism explaining dominance is environmental filtering: only species with a specific strategy are best adapted to the prevailing (high light) conditions and will dominate the young forest. As the forest gets older, biomass increases and a dense canopy prevents sunlight from entering the understory. The fierce competition for light means that trees need to specialize to make optimal use of different light-niches to be able to thrive here. Now dominant species need to be different from each other in terms of their light-capture traits, a mechanism known as competitively-driven limiting similarity. By exhibiting different strategies many species are able to co-exist in an environment that is increasingly packed by trees and limited in resources such as light.

During the first 25 years after agricultural abandonment the importance of environmental filtering as a driving force fades away rapidly and the importance of light gradient partitioning for species dominance starts to emerge. Understanding what factors shape species dominance is relevant as mainly the large dominating trees in an ecosystem determine how the forest functions.


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