Lay Summaries

The summaries below have been provided by our authors to help put their research paper into context for the wider scientific community and the general public. Lay summaries for the current issue, including our new Special Feature: Ecology of Organisms in Urban Environments are here. You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

 

Lay summaries for the current issue, including our new Special Feature: Ecology of Organisms in Urban Environments.

 

You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

 

 

How are leaf mechanical properties and water use traits coordinated by vein traits?—A case study in Fagaceae

Kiyosoda Kawai and Naoki Okada Hierarchal vein system in Quercus gilva (Fagaceae). Photo credited to authors..

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If you take a stroll into a forest, you will immediately find a variety of leaf shapes there. Broad-leaved (dicotyledonous) flowering plants (Angiosperms) are the most diversified in morphology and this is also true for leaf venation. But, venation in all Angiosperms shares one key property; a hierarchal vein system, i.e. many types (orders) of veins whose diameter and length are dramatically different (see attached image).

This system has been known for a long time, but its functional significance is still discussed. One fascinating explanation has been “division of labor”: thick but short primary and secondary veins transport sugars and water over long distances. On the other hand, thin and net-like minor veins distribute water and collect sugars produced by photosynthesis. But, earlier researches have not paid much attention to another important vein function: mechanical support to keep the light-intercepting leaf stable against gravity.

In this paper, we examined the contribution of leaf veins to leaf mechanical properties and water use and attempted to confirm the “division of labor” hypothesis in Angiosperm venation. For this purpose, we employed 8 Fagaceae species (oak/beech family) with a diversity of leaf shape, leaf habit and venation. We quantified mechanical properties (toughness) of leaves by tearing the leaf lamina and water relations by measuring conductance of leaf and water use efficiency (photo- synthetically gained carbon / loss of water). We measured vein and leaf traits to explain the variation of these functions. For vein traits, we measured vein density (vein length per unit area) for different order veins.

We found that different order veins were associated with different leaf functions. Primary and secondary vein density influenced leaf carbon cost and mechanical properties. In contrast, minor vein density is associated with leaf hydraulics. These results showed that the division of labor occurs in multiple leaf functions among contrasting vein orders. Further our study suggests the possibility that combinations of vein density of different orders could have led to the diversification of multiple leaf functions in the Angiosperms.

Image caption: Hierarchal vein system in Quercus gilva (Fagaceae). Photo credited to 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.

 

Female guppies reduce energetic costs of being harassed by males by becoming more efficient swimmers

Shaun S. Killen, Darren P. Croft, Karine Salin and Safi K. DardenImage provided by authors.

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Females and males of the same species are often in conflict over the frequency and timing of matings. Typically male reproductive success is limited by access to females and males of many species will try to overcome this using a number of behaviours, such as chasing and even attacking females in an attempt to gain a mating. These types of behaviours are considered sexually harassing as males are attempting to coerce females into mating with them. Females can spend a lot of energy avoiding males in these situations and can even be injured. To reduce these costs, one possibility is that females may be able to change their own behaviour or physiology in ways that reduce the negative energetic consequences of harassment, or allows them to more easily escape male coercion.

We studied this likelihood in a laboratory setting by housing female Trinidadian guppies (Poecilia reticulata) for several months with varying levels of male harassment that they would normally encounter in the wild. In the wild male guppies spend a large portion of their time chasing and harassing females in an attempt to mate with them. Females can attempt to avoid this harassment by rapidly swimming away from the male during pursuits.

After five months, females exposed to higher levels of harassment were able to swim much more efficiently, using less energy to swim at a given speed compared to those exposed to lower levels of harassment. It seems that prolonged increases in high-intensity swimming in females, caused by male harassment, leads to changes in the physiology or swimming mechanics of individual fish, which reduce costs of swimming. Indeed, females that experienced lower levels of harassment spent more time swimming with their pectoral fins extended, an indicator of an inefficient swimming technique.

These results show that female guppies can reduce the energetic costs of male sexual harassment through changes in their swimming physiology or technique. Increased swimming efficiency or performance could also allow female guppies to escape male coercion more easily, giving them more control over matings. An exciting opportunity now exists to examine the extent to which this phenomenon occurs in the wild.

Image caption: 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.

Mechanisms and consequences of facilitation in plant communities

Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning

Fabio Bulleri, John F. Bruno, Brian R. Silliman, and John J. StachowiczIntertidal stands of Cystoseira. Photo credit: L. Benedetti-Cecchi.

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Negative species interactions, such as competition, predation or parasitism have been traditionally envisioned as the main forces shaping patterns of species distribution and abundance. Theoretical and empirical research over the last two decades, bringing compelling evidence of the prominent role of positive species interactions (i.e., facilitation and mutualism) in structuring natural communities, has altered this view. Here we take a niche-based view of such positive interactions. The fundamental geographic niche is the physical space in which a species can develop self-sustaining populations if not constrained by negative biotic interactions. The realized niche, in contrast, represents the space actually occupied by a species after accounting for interactions with other species. Previous research has suggested that facilitation or mutualistic interactions can expand species’ realized niches by reducing the impact of negative, niche-shrinking species interactions or, indeed, expand the fundamental niche by allowing species to persist in environments that would otherwise be too physically stressful.

The effects on whole communities of generalized niche expansion due to facilitation have been little explored. In the presence of a foundation species (i.e. species that play a key role in structuring associated communities), facilitation-broadened niches could become less distinct (increased overlap among potential competitors), ultimately altering the intensity of competitive interactions among species. Facilitation, by broadening niches, could therefore limit species coexistence. However, niche overlapping might also be reduced when the foundation species is sufficiently patchy or creates new micro-environments that increase environmental heterogeneity.

Important implications for key areas of ecology arise from this conceptual framework. For instance, the extent to which facilitated species can persist in the face of climate changes by seeking refuge with facilitators depends on the degree of niche overlap and differences in competitive ability among potential beneficiaries. In addition, because facilitation can modify the strength of interactions among species, either by increasing niche overlap or altering environmental heterogeneity, it can also change the fundamental shape of the relationship between species diversity and ecosystem functioning. In summary, a mechanistic understanding of the effects of facilitation on species distribution, biodiversity and ecosystem functioning will require an assessment of how niche-broadening via facilitation changes the degree of niche overlap within a community.

Image caption: Intertidal stands of Cystoseira. Photo credit: L. Benedetti-Cecchi.
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.

 

Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment

Dima Chen, Jianjun Li, Zhichun Lan, Shuijin Hu, and Yongfei BaiSemi-arid grassland in Inner Mongolia of China (Image provided by Qingmin Pan).

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In many areas of the globe and especially in Asia, deposition of atmospheric nitrogen compounds (N) is expected to continue to increase. The dramatic increases in N inputs have wide-ranging ecological impacts on the biotic community, biogeochemical cycles, and greenhouse gas emissions. As one of the largest carbon effluxes between the atmosphere and terrestrial ecosystems, soil respiration plays a vital role in regulating the atmospheric CO2 concentration and climate on Earth. N inputs can affect soil respiration through two mechanisms or pathways: direct N impacts through enhancing soil N availability, and thus increasing plant productivity, and indirect impacts through modifying soil acidity. Yet, few studies have experimentally assessed the relative effects of increased N availability vs. soil acidification on below-ground carbon cycling in natural ecosystems. To address this issue, we conducted a 12-yr N enrichment experiment and a 4-yr complementary acid addition experiment in a semi-arid Inner Mongolian grassland. We found that soil acidification exerts greater control than soil N availability on soil respiration in grasslands experiencing long-term N enrichment, suggesting the need to include soil acidification in predicting terrestrial ecosystem carbon balance under future N deposition scenarios. We also found that N enrichment enhanced soil depletion of base cations such as calcium and magnesium in this semi-arid ecosystem, indicating that researchers and policy makers should also consider the long-term effects of N enrichment on element availability for plants, wildlife, and domestic livestock.

Image caption: Semi-arid grassland in Inner Mongolia of China (Image provided by Qingmin Pan).
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.

 

Mistletoe influences community seedfall patterns

Ana Mellado and Regino ZamoraIn this Mediterranean pineland, parasitized trees, constituting the only (or most abundant) nutritive resource offered on the canopy layer, are particularly noticeable for frugivorous birds. Frugivores respond to mistletoe patchiness by visiting parasitized trees preferentially to unparasitized ones, driving a differential deposition of mistletoe and co-fruiting species seeds towards parasitized trees. Photo by Ugo Mellone.

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Mistletoes are fleshy-fruited parasitic plants that dwell in forest canopies and show a strongly aggregated spatial distribution. Parasitized trees potentially concentrate fruit-eating bird activity in their canopies, where birds find food, places to perch, and protection against predators. Thus, seed-deposition patterns are expected to reflect the heterogeneity associated with the parasite. This becomes especially important in generalist dispersal systems; however, so far, we do not know the implications of mistletoe spatial heterogeneity for the seed-dispersal pattern of other plants that fruit at the same time.

In a Mediterranean pineland, we analyze the impact of Viscum album subsp. austriacum on the seed-deposition pattern of a bird-dispersed plant community, taking into consideration the spatial and temporal variability of environmental factors influencing the birds’ habitat use, such as fruit availability and forest tree density. For four consecutive years, we studied 55 pairs of trees parasitized and unparasitized by mistletoe, analyzing fruit availability, bird visits, and the bird-dispersed seed rain in selected trees.

As expected, fruit-eating birds responded to mistletoe heterogeneity by visiting parasitized trees preferentially to unparasitized ones, generating a differential deposition of mistletoe seeds on tree branches while dispersing seeds of co-fruiting species under the host canopy. Availability of understory fruits remained similar in patches of parasitized and unparasitized trees, but showed strong temporal fluctuations reflected in the seed rain. On the other hand, mistletoe was not only more copious in patches of parasitized trees, but their fruit crops varied little between years, making mistletoes reliable food resources likely to lead to consistency in fruit-deposition patterns.

In conclusion, mistletoes, by patchily growing in the canopy layer and concentrating bird-dispersed seeds underneath, can shape the spatial seed-deposition pattern of fleshy-fruited plants in the forest. Moreover, as seeds constantly reach the same deposition sites over long periods, the soil beneath the host canopy could become hotspots for community regeneration. In degraded areas, such mistletoe effects might be critical, possibly promoting recolonization and vegetation recovery through bird activity.

Image caption: In this Mediterranean pineland, parasitized trees, constituting the only (or most abundant) nutritive resource offered on the canopy layer, are particularly noticeable for frugivorous birds. Frugivores respond to mistletoe patchiness by visiting parasitized trees preferentially to unparasitized ones, driving a differential deposition of mistletoe and co-fruiting species seeds towards parasitized trees. Photo by Ugo Mellone.
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.

 

Interactions under novel global change scenarios: How does ozone affect the triple interaction grass-endophyte-herbivore?

Andrea C. Ueno, Pedro E. Gundel, Marina Omacini, Claudio M. Ghersa, Lowell P. Bush andMaría Alejandra Martínez-GhersaLolium multiflorum and Rhopalosiphum padi.

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As human impact on the environment increases, biological systems, from individuals to ecosystems, are consequently exposed to novel situations. It is especially relevant to understand how symbiosis of plants with beneficial microorganisms will respond to rising atmospheric pollutants.

Tropospheric ozone is a very dynamic pollutant gas associated with human activities that causes oxidative stress on living organisms. At the same time, it has been proposed that episodic exposure to ozone might elicit plant defense mechanisms, increasing tolerance to biotic factors such as herbivory and pathogens. However, we propose that if the plant defense is conferred by a symbiotic microorganism, the opposite effect might be expected. The symbiosis between cool season grasses and fungal endophytes, which live inside the grass leaves, is a defensive mutualism since host plants obtain resistance against herbivory mediated by several fungal alkaloids. Here we show that endophyte-symbiotic and endophyte-free plants of annual ryegrass exposed to ozone for just a few hours were differently affected. We evaluated the effectiveness of the defensive mutualism by exposing the plants to herbivory by aphids. We found that ozone impaired the resistance to aphids in endophyte-symbiotic plants but it slightly increased that of endophyte-free plants. In conclusion, our work suggests that the growing incidence of ozone as a novel stress factor under some global change scenarios could change the rules of certain symbiotic interactions in nature.

Image caption: Lolium multiflorum and Rhopalosiphum padi.
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.

 

Open wide! How and why gape reduces bite force in bats

Sharlene E. SantanaA Stripe-headed Round-eared Bat (Tonatia saurophila). Photo credit: Sharlene Santana.

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As the only flying mammals, bats completely rely on their skull and jaw muscles as major tools for grasping and processing food items. The outstanding diversity of bat diets, spanning fruits and insects of various sizes, to vertebrates and even blood, has resulted in the evolution of a plethora of cranial specializations that allow bats to bite with the appropriate amount of force and at the gapes necessary to consume their preferred foods. Theory predicts, however, that mammals experience trade-offs between their ability to produce a strong bite and to bite at wide gapes. First, opening the jaw at a wide gape stretches the fibers within jaw muscles, which makes their contraction weaker. Second, skull and muscle anatomies that allow for strong bites (e.g., short jaws, short muscle fibers) hinder the production of bite force at wide gapes, whereas anatomies that are more suited for biting at wide gapes (e.g., long jaws, long muscle fibers) are not optimal for producing strong bites.

Very few studies have confirmed these predictions in wild mammals, or harnessed the power of computer models to more deeply investigate this topic. This study documented the variation in bite force at low and wide gapes across free-ranging, tropical bat species, and built 3D computer models of their skulls to identify anatomical traits underlying the relationship between bite force and gape. Using these approaches, we corroborated that bites get weaker as bats have to open their mouth wider, but the drop in bite force varies substantially within and among species. In particular, bats that specialize in eating hard fruits experienced the steepest reduction in bite force at wide gapes. Computer models revealed that larger reductions in bite force at wide gapes are the product of a combination of anatomical features, including a shorter face, a larger temporalis (jaw closing) muscle, and a higher propensity for stretching this muscle during jaw opening. Altogether, these results suggest that gape-mediated changes in bite force can be explained both by behavior and cranial anatomy, and illustrate that these links are relevant for functional analyses of mammal diets.

Image caption: A Stripe-headed Round-eared Bat (Tonatia saurophila). Photo credit: Sharlene Santana.
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.

 

Swimming in UV

Ensiyeh Ghanizadeh Kazerouni, Craig, E. Franklin and Frank SeebacherManly Dam, image provided by authors.

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As pleasant as it is to swim in the sunshine, as humans we know very well how damaging UV radiation from the sun can be. It turns out that we are not the only ones affected by UV radiation: small fish (mosquitofish, Gambusia holbrooki) are too. Here we show that rather than causing sunburn, UV radiation affects the metabolism and capacity to move in fish. For example, exposure to UV-B radiation at relatively low levels reduces swimming endurance of fish by up to 30-40%. This can obviously have serious consequences for foraging behaviour, dispersal, and other ecological functions in these and probably other fish that are exposed to sunshine at the water surface. Luckily, evolution has found a solution to this problem. Fish that are born in summer when the water is warm and UV-B is high are much more resilient to the damage caused by radiation than fish that are born in winter. In other words, the early developmental conditions experienced by fish prepare them for the environment they encounter later in life. There is more to the story, though, because the characteristics of fish as well as many other animals are not fixed even within adults. The process of acclimation means that physiological functions can change reversibly within individuals and thereby lessen potentially negative impacts of environmental conditions. However, our data show that the capacity for acclimation is also dependent on developmental conditions. For example, fish born in summer can cope very well with UV-B but only when chronically exposed to their favourite temperature of 28oC; winter-born fish can barely acclimate at all. Our study reveals how complex the biological effects of environmental change are, with at least two of the major global climate drivers, temperature and UV, interacting in their impact on animals. Similarly, animal responses are a complex mix of genetics and development, which affects average characteristics of animals as well as their mutability later in life. These insights are important because they reveal how animals manage to do well in variable environments, and they will help us predict what the impacts of future climate change will be.

Image caption: Manly Dam, 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.

 

Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on a common milkweed

Tobias Züst and Anurag A. AgrawalThe milkweed aphids Aphis nerii and Aphis asclepiadis sharing their host plant, the common milkweed Asclepias syriaca. T. Züst.

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Herbivorous insect species strongly differ in the number of plants they feed on. Generalist herbivores are often very efficient at consuming plants and reproducing rapidly, but may be susceptible to toxins which the plant produces as defensive compounds. In contrast, specialized herbivores are generally more tolerant of plant toxins, and even may gain the ability to accumulate (sequester) plant toxins in their bodies as a defense against their own enemies. Understanding the effects of plant variation on herbivore performance is thus important for predicting population dynamics of herbivorous insects.

We compared the performance of four aphid species on a set of naturally variable common milkweed plants. Aphids reproduce clonally and the four species vary greatly in their diet breadths, while milkweed plants produce variable amounts of toxic cardenolides. Populations of the two more generalist species grew the fastest overall, and both species grew best on plants growing at a high rate, thus these species were likely limited by low resources on slower-growing plants. Food consumption of aphids increased with decreasing population growth, indicating decreasing resource-use efficiency with increasing specialization.

All four aphid species contained cardenolides in their bodies, but the amount of sequestered toxin increased with degree of diet specialization. Contrary to our predictions, the only species that was negatively affected by increasing levels of cardenolides in the host plant was the most specialized aphid, perhaps due to the very high levels of cardenolides accumulating in its body. The type of cardenolides accumulated in aphid bodies indicates a mostly passive mode of sequestration, with body cardenolide content being directly related to the rate of food consumption.

Generalist aphids performed best overall and were limited only by low plant growth but not by plant toxins. Specialist aphids were not affected by variation in plant growth but appeared to use resources less efficiently. Their increased food consumption resulted in higher cardenolide sequestration to the point of causing negative effects on population growth at the very highest levels. Variation in both growth rate and cardenolide levels of milkweed plants is thus likely to determine the relative distribution of generalist and specialist herbivores in the field.

Image caption: The milkweed aphids Aphis nerii and Aphis asclepiadis sharing their host plant, the common milkweed Asclepias syriaca. T. Züst.
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.

 

What features do plants use to survive drought?

Alexandria L. Pivovaroff, Sarah C. Pasquini, Mark E. De Guzman, Karrin P. Alstad, Jenessa S. Stemke, and Louis S. Santiago Photo by Louis Santiago.

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Tree mortality during drought has been documented in forests worldwide. It is thought that with global change, the frequency and intensity of extreme climatic events, such as drought, will increase. Although we have some information about the relative drought resistance of plant species, in many ecosystems, we still do not have a good physiological understanding of which species are most likely to die first. Physiologists are also currently trying to determine which mechanisms cause plants to die during drought. When water is limiting, plants can either close their stomata to conserve water at the risk of restricting photosynthetic carbon uptake, or they can open stomata to continue photosynthetic carbon uptake at the risk of losing too much water. Plants could therefore die of carbon starvation or hydraulic failure during drought, but which mechanism is more prevalent under what kind of conditions? And, what are the other traits that are important for maintaining internal carbon and water supplies during drought?

In this study, we measured seven drought survival traits to characterize how these traits combine in species and whether there were obvious drought survival strategies. We found that hydraulic architecture, the relative amount of water transport tissue and evaporative leaf surface area, was related to resistance of the stem tissue to water deficit. Yet, we also found that many traits occurred with no apparent pattern with regard to other traits, leading to a vegetation community with a large diversity of strategies for dealing with drought. This is likely because the study was conducted along a transition between two major vegetation types: California chaparral shrublands and the Mojave Desert. At the continental meeting of these two vegetation types, many species are on the edge of their range, so it is thought that areas such as the study site of this paper have a high chance of mortality during climate change. California is currently in a major drought, so if mortality begins to strengthen, the drought resistance characteristics studied in this paper should help us understand why certain species are dying and allow predictions for other sites.

Image caption: Photo by Louis Santiago.
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.

 

Butterfly males can smell the mating status of females and use this information to design their ejaculate

Helena Larsdotter-Mellström, Kerstin Eriksson, Niklas Janz, Sören Nylin and Mikael A. CarlssonImage provided by authors.

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One of the most fascinating aspects of sexual selection is sperm competition. In many species, females mate with several partners, causing competition among sperm from the different males. One option for the males to maximise the number of fertilizations is to increase the size of the ejaculate. A large ejaculate would however be a more important investment when mating with an already mated female than with a virgin. Therefore, it would be beneficial for males to be able to assess the female mating history and accordingly adjust the size of the ejaculate.

So how can the male assess the mating status of a female? There is evidence that many animals can use odour cues, pheromones, for this purpose. A previous study showed that males of the Green Veined White butterfly, Pieris napi, transfer an anti-aphrodisiac signal, methylsalicylate, to females together with sperm at ejaculation. This compound signals to other males that the female is already mated, making her less attractive as a partner. Here, we asked if males may also use this signal to tailor the ejaculate accordingly, i.e. transfer more sperm to an already mated female than to a virgin.

We could show that males have a sense of smell that can distinguish between different concentrations of methylsalicylate. Females also have this ability but are less sensitive to it.

Next we found that males transferred a larger ejaculate to mated females than to virgins. But most interestingly, males also transferred a larger ejaculate to virgin females with artificially added anti-aphrodisiac.

Thus, we have shown a mechanism for how males can assess the mating status of females and we have furthermore shown that they can use this signal to tailor their ejaculates.

Image caption: 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.

 

Breath of death: how a parasite favours its transmission through hijacking its host’s hypoxia-acclimation processes

Marie-Jeanne Perrot-Minnot, Matthieu Maddaleno, Frank Cezilly The thorny-headed worm Polymorphus minutus : larvae dissected from the crustacean host, and infective to the definitive host, a waterbird.

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Parasites with complex life cycles, involving more than one host, often alter the behaviour of their intermediate hosts in ways that increase their chances of getting transmitted to final hosts. For instance, the thorny-headed worm Polymorphus minutus is known to induce ‘reversed geotaxis’ in its amphipod host Gammarus roeseli, such that infected hosts swim closer to the water surface and presumably become more vulnerable to predation by aquatic birds (in which the parasite will complete its life cycle).

So far, the mechanisms underlying host manipulation by parasites remain poorly known. As hypoxia (shortage of oxygen) in aquatic invertebrates is known to induce complex physiological responses and reversed geotaxis, we conjectured that the reversal of geotaxis induced by P. minutus in amphipod hosts could result from a hypoxia-like state through two potential mechanisms. First a decrease in the metabolic rate of amphipods could be directly caused by infection with P. minutus. Second, the parasite could mimic a state of hypoxia in its host, as P. minutus has been previously shown to excrete both lactate and succinate (two end-products of its own anaerobic metabolism).

Under hypoxia, uninfected G. roeseli showed negative geotaxis and lower metabolic rate, two traits altered by infection with P. minutus, albeit with different intensities. The injection of a mixture of lactate and succinate in uninfected amphipods also mimicked the parasite-induced reversion of geotaxis, without affecting metabolic rate. In addition, both P. minutus-infected gammarids and uninfected ones conditioned to hypoxia for two days showed elevated levels of lactate in the brain, but not in the haemolymph (the fluid analogous to blood in vertebrates). Overall, our results strongly suggest that the pathways involved in anaerobic metabolism and hypoxia-signalling might be responsible for the changes in geotaxis and metabolic rate induced by P. minutus infection.

This study emphasizes the need to consider the tight and complex connections between physiological processes and behavioural adjustments, in particular at the brain level, in the understanding of parasitic manipulation, and more broadly of behavioural changes in infected hosts.

Image caption: The thorny-headed worm Polymorphus minutus : larvae dissected from the crustacean host, and infective to the definitive host, a waterbird.
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.

 

Are elephant seals optimal divers?

Joffrey Jouma’a, Yves Le Bras, Gaëtan Richard, Jade Vacquié-Garcia, Baptiste Picard, Nory El Ksabi and Christophe GuinetFemale elephant seal and her pup on Kerguelen Island. Photograph by Joffrey Jouma’a.

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Optimal foraging theory offers a conceptual framework to describe and understand behavioural strategies adopted by an animal to maximise its fitness. Based on the optimisation principle, this theory aims to predict the best strategy for maximising efficient foraging under energetic and temporal constraints, e.g. where is the best place to feed on, what is the best type of prey to catch, and when to switch from one patch to another? Because marine predators must find prey in three dimensions and air-breathing divers are forced to come up to the surface to renew their oxygen store, several adaptations need to be considered to study foragers in a marine context. Things are twice as difficult, because only a few studies deal with the optimal theory applied to diving predators, and even fewer have tested in situ the associated assumptions. Here, we focus on the Southern Elephant Seal, a nearly continuous diver that can however be easily equipped with Time-Depth-Recorders (TDR) due to its annual presence on land for reproduction. Using TDR associated with accelerometers provides information on diving behaviour, such as the time spent in the foraging zone, the swimming effort or even the number of prey catch attempts. Accelerometers are a powerful tool that can also tell us about the animal’s buoyancy. We showed that elephant seals adjust precisely their time spent in the foraging zone with the depth targeted, their body condition, but also with prey encounter rate. For instance, an animal with a high body density will usually tend to stay less time in the foraging zone due to the energy required to come up to the surface. This study also highlights that using only the time spent in the foraging zone to estimate foraging success can be seriously misleading in the Southern Elephant Seal. Indeed, a long time spent in the foraging zone suggests a strong foraging success for shallow depths (>300 m), whereas at greater depths foraging success is lower.

Image caption: Female elephant seal and her pup on Kerguelen Island. Photograph by Joffrey Jouma’a.
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.

 

Nonlinear responses of ecosystem carbon fluxes and water use efficiency to nitrogen addition

Dashuan Tian, Shuli Niu, Qingmin Pan, Tingting Ren, Shiping Chen, Yongfei Bai and Xingguo HanView of typical steppe, Inner Mongolia, China (left) and experimental site of nitrogen addition (right). Photo by Qingmin Pan.

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Human activities (e.g. fertilization and fossil fuel combustion) have greatly altered the global nitrogen cycle, leading to widespread reactive nitrogen inputs (nitrogen deposition), which may have profound impacts on ecosystem processes (e.g. biomass production, carbon and water cycles) and services. Therefore, it is an urgent task for scientists to explore how such elevated nitrogen inputs affect ecosystem processes. However, most previous simulation experiments dealing with the influences of nitrogen deposition on ecosystem carbon and water cycles used only two discrete levels of nitrogen treatment (i.e. with and without addition of nitrogen), which cannot reveal the likely nonlinear response of these processes to continuous nitrogen deposition in terrestrial ecosystems.

The Eurasian steppe is the largest remaining natural grassland in the world, and is subjected to increasing levels of nitrogen deposition. To evaluate the impacts of nitrogen enrichment on ecosystem functioning in this grassland ecosystem, we have started a long-term nitrogen addition experiment with multiple nitrogen input levels in a typical steppe ecosystem in Inner Mongolia of China, a representative area of Eurasian steppe, since 2000. In the current study, we focused on the responses of carbon and water processes to a gradient of nitrogen addition. We showed that both ecosystem carbon uptake and ecosystem respiration followed nonlinear patterns with increasing levels of nitrogen addition, and specifically that the magnitude of nitrogen-induced increases in these processes declined at high nitrogen levels relative to those at low nitrogen levels. In contrast, ecosystem-level water flux was not greatly affected by nitrogen addition. Therefore, the response patterns of ecosystem water use efficiency, the ratio of carbon uptake to water loss, were mainly determined by carbon rather than water processes. These findings have important implications for predicting the changes in ecosystem carbon and water balance under future nitrogen-enriched scenarios and for the management of the world’s largest natural grassland.

Image caption: View of typical steppe, Inner Mongolia, China (left) and experimental site of nitrogen addition (right). Photo by Qingmin Pan.
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.

 

Small but active – pool size does not matter for carbon incorporation in belowground food webs

Johanna Pausch, Susanne Kramer, Anika Scharroba, Nicole Scheunemann, Olaf Butenschoen, Ellen Kandeler, Sven Marhan, Michael Riederer, Stefan Scheu, Yakov Kuzyakov and Liliane RuessConnectedness food web visualizing qualitative feeding relationships in the investigated arable soil (Photo credit: B. Lang).

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Soils store approximately 80% of global terrestrial carbon (C) and small changes of fluxes into and out of this pool may influence the atmospheric CO2 concentration and interact with climate change. Soil food webs are important drivers of major ecosystem functions such as C and nutrient cycling, and hence they play a central role in soil fertility as well as in C stocks. Despite this importance, the cryptic soil habitat and the complex interplay between multitudes of organisms hamper the understanding of C and energy fluxes through the soil food web.

Carbon resources enter the soil as shoot- and root-litter after plant death and as organic compounds released by living roots (rhizodeposits). In particular in agroecosystems, where aboveground plant biomass is harvested, C dynamics are largely controlled by the input of rhizodeposits. Rhizodeposits contain various substances that can easily be utilized as C and energy source by bacteria and fungi and are passed on to higher trophic levels.

To follow the flux of rhizodeposits into the food web of an arable system, maize plants were exposed to 13C-enriched CO2. 13C is a natural isotope of carbon, usually occurring in low amounts in the environment. After 13CO2 assimilation by plants, we followed the release of C from living roots into the soil and into various food web members. These were microorganisms (bacteria and fungi), microfauna (nematodes – small roundworms), mesofauna (mites and springtails) and macrofauna (spiders, beetles).

In contrast to general views we showed that the flux of root-derived C in soils is not necessarily driven by pool size, i.e., by food web members with large C stocks. Instead, members with small pool size but with high turnover rates (growth and death) dominate the C flux through the food web. This becomes evident at our arable site where easily available rhizodeposits are predominantly utilized by fungi and channelled through the fungal energy pathway to higher trophic levels. Our findings disprove the widely held idea of the dominance of the bacterial-energy channel and showed the importance of the fungal-energy channel for belowground utilization of root-derived C in arable soil.

Image caption: Connectedness food web visualizing qualitative feeding relationships in the investigated arable soil (Photo credit: B. Lang).
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.

 

Nutrient foraging behaviour of four co-occuring perennial grassland plant species alone does not predict behaviour with neighbours

Gordon G. McNickle, Michael K. Deyholos, and James F. Cahill Jr.A pot with one individual of each of the four species competing in soil.

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To the untrained eye plants might appear to be more like inanimate objects than organisms that exhibit complex behavioural responses or engage in competitive games with neighbour plants. However, like any living organism, plants must solve problems in a world full of complex and ever changing stimuli. A plant that does respond adaptively to these changing stimuli should outperform a plant that does not. Indeed, if you know where to look, you will find that plants are remarkably good at assessing and responding to a variety of stimuli in ways that are often best described using behavioural models.

Here, we explored what has become known as the nutrient foraging behaviour of plants either growing alone or with neighbours. When plants are alone, it is well established that their foraging behaviour is to place more roots into nutrient rich patches than they do in nutrient poor patches. However, it is less well understood how plants forage in the presence of other plants that are competing for those nutrients in soil. We showed that the behaviour of plants grown alone does not predict the behaviour of plants grown with neighbours. Instead, plants grown with competitors engage in a sort of arms race for nutrients under competition: they produce more total roots in the presence of competitors than they do when grown alone. Broadly speaking this is a result that is predicted from game theory. Plants are playing games with each other!

Image caption: A pot with one individual of each of the four species competing in soil.
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.

 

Visual and odour cues: how plants change after herbivore damage and pollination

Dani Lucas-Barbosa, Pulu Sun, Anouk Hakman, Teris A. van Beek, Joop J.A. van Loon and Marcel DickeA Hoverfly visiting a Black Mustard flower. Photograph credits: Dani Lucas-Barbosa.

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Plants in nature interact with many antagonistic organisms, such as insects that feed on them, and beneficial organisms, such as carnivorous and pollinating insects. To defend themselves against plant-feeding insects, plants can, for instance, produce odours that can be used by carnivores to find their herbivorous prey. However, odours that plants produce upon herbivore attack may repel pollinators that help the plant to reproduce, by carrying pollen from one flower to another. Thus, the attraction of pollinators may conflict with attraction of carnivorous insects. In this study, we investigated the role of plant chemistry in such a conflict. We assessed how plant chemistry changes after pollination or to damage by herbivores, and how this affects the behaviour of flower visitors. In terms of plant chemistry, we investigated how the production of odours and visual cues changes after the plant has been pollinated, and exposed to herbivore damage. Both herbivores and pollinators elicit important changes in the chemistry of flowers. Black mustard plants indeed change their odour production as well as the production of compounds that can confer colour to flowers, after having been pollinated or exposed to insect damage, or even to both. Our results show that butterflies use different cues when searching for a plant to deposit their eggs, or for a flower to feed from. Changes in chemistry, following pollination, influenced the behaviour of butterflies that feed on nectar, but not that of hoverflies that collect pollen from the flowers. We discuss the results in the context of the trade-off between plant defence and pollinator attraction, and suggest that changes after herbivory can interfere with changes after pollination. Therefore, these responses must be addressed in an integrated way because, in nature, plants are exposed to herbivores and pollinators at the same time.

Image caption: A Hoverfly visiting a Black Mustard flower. Photograph credits: Dani Lucas-Barbosa.
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.

Mechanisms and consequences of facilitation in plant communities

The dark side of facilitating grasses

Richard Michalet, Christian Schöb, Sa Xiao, Liang Zhao, Tuo Chen, Li-zhe An and Ragan M. Callaway Cushion of Thylacospermum caespitosum facilitating beneficiary species in the Qilian Shan range (China).

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In stressful environments, such as the high alpine, plants often benefit from each other’s presence. For example, shrubs or plants with so-called cushion morphologies ameliorate the most stressful conditions in the high alpine by providing substrate for other plants to root and providing access to water and nutrients. Such positive effects of cushion plants for other plant species are very widespread in the alpine and an important process to sustain alpine biodiversity. However, the close co-occurrence of these other, so-called beneficiary species with the cushion plant may feed back to the benefactor cushion and influence their fitness. This feedback effect of the beneficiary species on the benefactors is still poorly understood. In this study we show that grasses associated with benefactor cushions have a negative feedback effect on cushions, whereas other associated species, such as other herbaceous species and shrubs don’t. Some of our results even demonstrated positive feedback effects of herbaceous plants on the cushion, indicating some sort of symbiosis. In contrast, the grasses acted more like parasites of the cushions. In addition, since we replicated this study at over 30 sites across the globe, we could also demonstrate that this negative effect of grasses on the benefactor cushions was strongest under dry environmental conditions. This suggests that the co-occurrence of grasses and the cushion plant increased competition for water among them, thereby reducing the fitness of the cushion. As a consequence, while earlier studies showed that beneficiary species have mostly a negative feedback effect on their cushion benefactors, with this study we could show that it is in particular the grasses that are responsible for this ‘cost’ of facilitation by the cushion plants.

Image caption: Cushion of Thylacospermum caespitosum facilitating beneficiary species in the Qilian Shan range (China).
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.

Review

Macrophysiology – a decade of novel insights

Steven L. Chown and Kevin J. GastonTiliqua rugosa (sleepy lizard) in a South Australian agricultural landscape. Macrophysiology provides a means to understand life’s responses to such impacts at broad scales.

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The investigation of variation in physiological characteristics over large geographic and temporal scales, and the ecological and evolutionary implications of this variation, has now been undertaken, as a defined field, for a decade. Known as ‘macrophysiology’ the field has contributed substantially to our understanding of the world. A notable example is the demonstration that geographic variation in the ability of animals to tolerate high temperature is much less pronounced than geographic variation in responses to low temperature. Moreover, it appears that environmental temperatures are close to tolerances in tropical and subtropical areas. In consequence, climate change may be especially problematic for species from the tropical and mid-latitudes. These concerns have now made their way into conservation policy.

This review provides a range of other examples of progress realized by the field, and then shows how macrophysiology can further help to address some of the most pressing modern challenges of environmental change. It also shows just how similar evolved responses to the environment are in plants and animals, though the benefits of comparing these groups have yet to be fully realized. We identify 10 key challenges for macrophysiology. These include better understanding of geographic variation in organismal characteristics, understanding how small scale climate variation affects plants and animals, working out how multiple interacting factors might influence populations, and exploring how modification of landscapes by urban areas and agriculture has affected plant and animal environmental responses.

We provide a comprehensive overview of the current standing of the field and its future prospects, giving any newcomer immediate access to its conceptual and methodological foundations. Easy access to the full range of work in the field is also provided along with rich graphic illustrations of its relationships to other areas of biology and the insights it has delivered.

Image caption: Tiliqua rugosa (sleepy lizard) in a South Australian agricultural landscape. Macrophysiology provides a means to understand life’s responses to such impacts at broad scales.
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.

 

Experimental reduction of hematocrit affects reproductive performance in European starlings

Raime B. Fronstin, Julian K. Christians and Tony D. WilliamsEuropean starling. Image provided by authors.

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Hemoglobin plays a critical role in the transport of oxygen from the lungs to the tissues. It is therefore widely assumed that hemoglobin levels and hematocrit (the proportion of blood volume occupied by red blood cells) are positively related to aerobic performance. Indeed, in birds, hemoglobin and hematocrit increase during aerobically demanding periods such as migration. However, hematocrit and hemoglobin levels generally go down during egg production in female birds, and this decrease can be similar in magnitude to the increases associated with activities such as migration. Furthermore, these decreases can persist beyond egg production, into incubation and chick-rearing. Why would females decrease their aerobic capacity just before they have to gather food for their offspring? One hypothesis is that the decrease in hematocrit is caused by the increased estrogen levels needed to produce eggs. This could potentially mean that estrogen creates a non-resource based trade-off (i.e. one that does not depend on competition for a limiting resource) between egg production and chick-rearing. Such a trade-off would be novel and intriguing, but its existence hinges on the assumption that decreased hematocrit will adversely affect reproductive performance. To address this question, we treated free-living female European starlings (Sturnus vulgaris) with phenylhydrazine (PHZ), which destroys red blood cells. Females treated with PHZ after the removal of their first clutch took longer than controls to produce a replacement clutch, but there were no other effects on measures of reproductive performance. Females treated with PHZ during incubation had chicks that were lighter at hatch. Furthermore, in one of two years, females treated with PHZ during incubation produced fewer and smaller fledglings. The year in which PHZ affected fledgling size and number was a particularly difficult year (low annual productivity) based on other data. Our results suggest that the decrease in hematocrit that routinely occurs during egg production may exert costs on subsequent stages of reproduction, but that these costs may be exacerbated when ecological conditions are poor.

Image caption: European starling. 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.

 

Climate-induced collapse of a tropical predator-prey community

Beata Ujvari, Gregory Brown, Richard Shine and Thomas MadsenBeata Ujvari and Thomas Madsen catching water pythons in the “good old days” when the snakes were common.

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If climate change threatens wildlife populations, will that be by gradual shifts in mean condition such as rainfall and/or temperature, or by increased frequency of extreme weather events? Based on long-term data (from 1991 to 2014), the aim of the present study was to analyze and compare the responses of predator (water pythons, Liasis fuscus ) and prey (dusky rats, Rattus colletti ) to extreme climatic events versus normal, albeit highly variable, climatic conditions in the Australian wet-dry tropics. From 1991 to 2005, water pythons and dusky rats showed significant climate-driven fluctuations in numbers, and annual fluctuations in rat numbers generated a corresponding variation in female python reproductive output (recruitment). Our analyses showed that annual variation in recruitment was the main factor in driving the annual variation in water python numbers. The fluctuations in rat and python numbers recorded from1991 to 2005 were, however, trivial compared to the impact of two massive but brief (24 h) deluges in 2007 and 2011. The two extreme weather events resulted in massive and rapid flooding of the dusky rat’s habitat which drowned virtually the whole rat population. As dusky rats constitute the water python’s main prey, the two floods have resulted in the pythons experiencing an unprecedented famine in 7 out of the last 8 years. The virtual lack of prey has resulted in a significant reduction in python feeding rates, reproductive output, growth rates, condition, survival, body length and importantly in python numbers, from a high of 3173 snakes recorded in 1992 to 96 in 2013. Our results demonstrate that attempts to predict animal responses to climate change, even if based on long-term studies, may be doomed to failure. Consequently, biologists may need to confront the uncomfortable truth that increased frequency of brief unpredictable bouts of extreme weather can influence populations far more than gradual deviations in mean climatic conditions.

Image caption: Beata Ujvari and Thomas Madsen catching water pythons in the “good old days” when the snakes were common.
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 tadpole competition affects frog guts and feeding

Sarah S. Bouchard, Chelsea R. Jenney O’Leary, Lindsay J. Wargelin, Julie F. Charbonnier, and Karen M. WarkentinRed-eyed treefrog, Agalychnis callidryas, metamorph.  Photo credited to Karen M. Warkentin.

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The transformation of an aquatic, herbivorous tadpole into a terrestrial, carnivorous frog is a striking example of metamorphosis, involving coordinated changes in many body parts. Legs grow, the tail is absorbed, and the tiny tadpole mouth becomes the broad mouth of a frog. The digestive system, particularly the intestine, is also dramatically remodeled for the frog’s new diet, shrinking in length by about 80%. During the aquatic tadpole stage, digestive systems also vary. In ponds teeming with tadpoles, where individual tadpoles compete for food, they develop very long guts that help them extract more nutrients from their food. Despite this, they grow slowly and emerge from the water as small frogs. In contrast, when tadpoles are few and far between and food is abundant, they invest less in intestines, but are still able to grow fast and leave the water as large juvenile frogs. In the red-eyed treefrogs of Central American rainforests, small frogs that emerge from competitive pond environments grow quickly after metamorphosis, whereas large ones from resource-rich ponds grow slowly once on land. In this research we asked why, specifically testing the hypothesis that initial differences in tadpole guts, despite their radical shortening during metamorphosis, might partially persist to affect frog feeding and growth on land. We raised tadpoles in large outdoor tanks with either high or low levels of competition. Low tadpole competition resulted in big, fat frogs that took nearly two weeks after metamorphosis to begin feeding regularly. High tadpole competition produced very small, skinny frogs that were one third the size of the larger frogs. These small frogs began feeding at a high level even before they finished absorbing their tadpole tails. Despite large differences in body size, small frogs had the same length guts as large frogs. This means that differences in tadpole guts do persist after metamorphosis, despite the extensive remodeling that takes place.

Their relatively large guts allow very small frogs to eat the same amount of food as large frogs without sacrificing digestibility. Together, long guts and high feeding rates help explain why small juvenile frogs grow faster than large ones.

Image caption: Red-eyed treefrog, Agalychnis callidryas, metamorph. Photo credited to Karen M. Warkentin.
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.

 

Immune response in breeding elephant seals

Hannah E. Peck, Daniel P. Costa and Daniel E. CrockerFemale northern elephant seal with suckling pup. Photo provided by authors.

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Mounting an immune response to infection requires substantial energy. During reproduction, animals must balance the energy requirements of investing in their offspring with the energy required for immune responses that will insure their health and survival. Some animals, known as capital breeders, leave their food resources during reproduction and used stored body reserves to supply these energy costs. Little is known about the impact of capital breeding strategies on the ability to resist infections in mammals. Northern elephant seals forage in the marine environment, breed in dense terrestrial colonies, and exhibit high rates of milk production while fasting completely from food. Their body reserves strongly influence how much milk they give their pups. Mobilizing fat for milk production requires elevation of cortisol, a stress hormone that frequently suppresses the immune system in other animals. We characterized their ability to resist infection by measuring a suite of immune markers in 197 blood samples from elephant seals at the beginning and end of their breeding and moult haul-outs on land. We explored impacts of breeding, body condition, and plasma cortisol on the ability to fight infections while on shore.

Immune system responses were greater and more varied among individuals during breeding. Body mass and fat reserves had positive associations with the ability to fight infections. A marker for the ability to resist infection by parasites was lower in animals with higher cortisol. These data show that coming together in dense breeding colonies increases the risk of infection and that committing energy to milk production while fasting reduces the ability of mothers to fight these infections. Elephant seal mothers need to balance the energy required to stay healthy and survive with the energy needed to make milk and produce healthy pups.

Image caption: Female northern elephant seal with suckling pup. 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.

 

Structure and functioning of intertidal food webs along a shorebird flyway

Teresa Catry, Pedro M. Lourenço, Ricardo J. Lopes, Camilo Carneiro, José A. Alves, Joana Costa, Hamid Rguibi-Idrissi, Stuart Bearhop, Theunis Piersma and José P. GranadeiroShorebirds gather in large numbers at tidal flats of Bijagós archipelago, Guinea-Bissau.

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Shorebirds are long distance migrants which during the non-breeding season depend on an intercontinental network of extremely diverse coastal wetlands at temperate, sub-tropical and tropical latitudes. In these wetlands, shorebirds gather in huge numbers and mostly feed on macroinvertebrates (e.g. worms, crustaceans and molluscs), playing a key role as predators in local food webs. These food webs include the whole network of trophic interactions among all co-existing organisms, as well as the transfer of nutrients and energy (trophic pathways) from its basal sources (e.g. plants) to primary consumers (e.g. macroinvertebrates) and their predators (e.g. shorebirds). Structure and dynamics of food webs depend on an extensive range of biotic and abiotic conditions which might vary considerably among areas.

In our study we characterized food webs using a set of community metrics based on stable isotopes. Stable isotopes (such as carbon δ13C and nitrogen δ15N) can inform the trophic ecology of consumers (i.e. what eats what), given that isotopic composition in tissues of consumers is directly linked with their diet. We compared the structure and functioning of food webs in four tidal ecosystems along a shorebird flyway: Tejo estuary (Portugal), Sidi Moussa (Morocco), Banc d’Arguin (Mauritania) and Bijagós archipelago (Guinea-Bissau). Our results suggest that food web structure is shaped by the number of trophic pathways of organic matter transfer. Indeed, the food web of Banc d’Arguin was characterized by lower trophic diversity and higher functional redundancy (higher number of community members with similar trophic roles) than the other sites, which might be related to the lack of inputs from both freshwater and nutrient-rich offshore oceanic waters.

There were also differences in the organization of shorebird communities among the study areas, which were largely coincident with the patterns found for the whole food webs. Shorebird communities of Banc d’Arguin and Bijagós archipelago showed comparatively low inter-specific niche overlap, which might result from species differently exploiting available resources. As tropical systems typically offer comparatively lower harvestable prey biomass for shorebirds, niche partitioning can be a strategy to reduce inter-specific competition. While our results highlight the trophic plasticity of species inhabiting areas with distinct environmental conditions, they also suggest that shorebirds’ community structure might serve as a proxy to describe the overall structure of tidal food webs.

Image caption: Shorebirds gather in large numbers at tidal flats of Bijagós archipelago, Guinea-Bissau.
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.

 

Assessing the ability of flies to adapt to heat

Sandra Hangartner and Ary A. HoffmannDrosophila melanogaster. Photo provided by authors.

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Average temperatures are now predicted to increase by 2-4°C by the end of the century and extreme temperatures are expected to increase even further. This can threaten the survival of species if their upper thermal limits are repeatedly exceeded. Whether animals have the capacity to evolve to adapt to increasing temperatures is widely debated but still poorly understood. One of the limitations of work carried out to date is that resistance to extreme temperatures has been measured in different ways, but the relationships between components of resistance measured by these different methods is unclear.

The fruit fly, Drosophila melanogaster, has been extensively used to study thermal resistance. Previous studies have produced inconsistent results on its evolutionary capacity to increase upper thermal tolerances. We have therefore re-examined this issue using the powerful approach of selection experiments. These experiments also allow us to test the extent to which resistance can be altered and whether different components of resistance are connected or independent.

To undertake selection, we exposed the flies to high temperatures in each generation and then selected the most heat resistant flies. We also kept flies as control populations which were not exposed to any heat stress. After more than ten generations of strong selection, we tested for differences between the selected and control populations. We found that the selected flies had evolved higher heat resistance in all components measured, but the increase in resistance amounted to no more than 0.5°C. We also showed that these changes did not depend on the way in which resistance was measured.

These results suggest that while D. melanogaster flies have some evolutionary potential to become more resistant to heat, there are limits to this potential. The level of evolution detected here may be insufficient to keep up with temperature increases predicted under climate change. If evolution of upper thermal tolerance is also similarly constrained in other species, then those species that live at temperatures near their upper tolerance limit may be at a particularly high risk of extinction following climate change.

Image caption: Drosophila melanogaster. 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.

 

Individual plasticity of fish metabolic rate

Tommy Norin, Hans Malte and Timothy D. ClarkJuvenile barramundi. Photo by Timothy Clark.

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Metabolic rate can vary substantially between individual fish of the same species, size, and sex, with some individuals metabolising energy 2-3 times faster than others. This between-individual variation can have considerable ecological and evolutionary consequences as it is associated with variations in growth and other important life history traits. However, almost nothing is known of how this diversity in metabolism is impacted by the dynamically changing conditions of the natural environment. We first measured how individual barramundi, a tropical fish inhabiting estuaries and tidal creeks in Australia, differed in their resting and maximum metabolic rates, as well as in their metabolic scope for various energy-demanding tasks (termed aerobic scope) under acclimation conditions (35 ppt salinity, 29oC, 100% air saturation). Subsequently, we determined how differences in these metabolic attributes were related to the individual fish’s metabolic response (i.e. their change in metabolic rate) when faced with environmental changes in salinity, temperature, and oxygen availability. We found a close relationship between the metabolic attributes of the individual fish at their acclimation conditions and how much the fish changed their metabolic rates when environmental conditions were altered. Individuals that had elevated metabolic attributes under acclimation conditions showed little change in resting or maximum metabolic rate and aerobic scope in response to low salinity (10 ppt) and high temperature (35oC), but maximum metabolic rate and aerobic scope were greatly depressed by low oxygen availability (hypoxia; 45% air saturation). In contrast, individual barramundi with low metabolism under acclimation conditions displayed a substantial increase in resting and maximum metabolic rates, as well as in aerobic scope, in response to high temperature and (to a lesser extent) low salinity, but hypoxia had very little effect. These findings highlight the diversity of physiological responses to environmental change within a population by showing how individual fish can remain metabolically insensitive to one environmental stressor at the cost of being highly sensitive to another. This suggests that possession of certain physiological traits may be advantageous in dynamically changing habitats, depending on the combination of environmental challenges being faced.

Image caption: Juvenile barramundi. Photo by Timothy Clark.
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.

 

Why do lizard dewlaps glow?

Leo J. Fleishman, Brianna Ogas, David Steinberg and Manuel LealA glowing dewlap. Photo Credit: Manuel Leal. The lizard Anolis lineatopus inhabits shaded forests throughout the island of Jamaica.  Territorial males extend a colorful throat fan – the dewlap – in visual displays that attract females and repel male rivals. The dewlap is translucent: it transmits and diffuses light striking its back surface.  In this picture the sun is located behind the animal, and the sunlight transmitted through the dewlap makes it appear to glow.  The translucent properties of the dewlap make its colors more vivid and easier to see.

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Many animals use impressive color patterns to communicate with other members of their species. Since most animals do not produce light themselves, these colored surfaces are only visible because they reflect natural light. In bright sunlight, reflected colors often appear intense and brilliant. In heavily shaded habitats, where most of the sunlight is blocked, the same colors often appear much duller, and different colors can be difficult to tell apart.

Anolis lizards are well known for their use of a colorful, expandable throat fan, called the dewlap, to attract mates and repel rivals. There are hundreds of species of anoles. They are active only during the day, but many species live in heavily shaded forest habitats where colors can be difficult to see. The dewlap is a very thin structure, and for this reason, some of the light that strikes its surface transmits through it, becoming colored and spreading in all directions as it does. If strongly lit from behind – for example when the sun is on the opposite side of the dewlap from the viewer – the dewlap appears to glow brilliantly, because the light passing through it is made colored and diffuse by the pigments in the dewlap. A color pattern of this type is referred to as translucent.

We explored the reasons why some species of anoles have evolved translucent dewlaps. Those with the most translucent dewlaps live in shaded forest habitats, where light levels are relatively low. When an anole opens its dewlap much of the light striking the back surface (opposite the viewer) passes through the dewlap. This adds to the light reflected back from the front surface (facing the viewer) and greatly increases the total light intensity reaching the viewer’s eyes. This makes the dewlap color much easier to detect, and to distinguish from other colored objects in the habitat. Mates and rivals can, therefore, quickly detect and identify the species of the displaying animal. This is the first study to demonstrate the evolutionary advantage of possessing a translucent display organ that utilizes diffuse transmitted light to increase its visibility.

Image caption: A glowing dewlap. Photo Credit: Manuel Leal. The lizard Anolis lineatopus inhabits shaded forests throughout the island of Jamaica. Territorial males extend a colorful throat fan – the dewlap – in visual displays that attract females and repel male rivals. The dewlap is translucent: it transmits and diffuses light striking its back surface. In this picture the sun is located behind the animal, and the sunlight transmitted through the dewlap makes it appear to glow. The translucent properties of the dewlap make its colors more vivid and easier to see.
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 or watch a video on this reserach below:

Mechanisms and consequences of facilitation in plant communities

Plants helping plants for sustainable agriculture

Rob W. Brooker, Alison J. Karley, Adrian C. Newton, Robin J. Pakeman and Christian Schöb Harvesting a study of the impact of barley mixtures on rare and common weed species.

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Plant competition is the negative interactions that occur when two plants try to use the same pool of resources such as nutrients, particularly when that pool is only of limited size. The opposite of plant competition is plant facilitation, which occurs when one plant has a beneficial effect on its neighbour, for example by providing it with some kind of nutrient that it would otherwise lack, or sheltering it from extreme environmental conditions or the attentions of herbivores. Recently there has been a remarkable increase in our understanding of plant facilitation, particularly in more severe environments such as arctic, alpine or desert ecosystems.

However, in this paper we describe how facilitation could play an important role in making agricultural systems – particularly crop systems – more sustainable. We look at three main groups of beneficial interactions. First we briefly discuss the beneficial interactions that occur between different crop species in intercropping systems. Second we consider beneficial interactions between different varieties (genotypes) of the same crop species – these underpin what are known as crop mixture effects. In both cases many of the benefits come from maintaining crop yields whilst reducing the use of agricultural chemicals. Third we describe new research which suggests that some rare plant species may depend directly on crops for their survival.

We end by considering how we can link our ecological understanding of facilitation in crop systems to new management practices that might benefit biodiversity. In some cases no work is needed: intercropping and variety mixtures are already widely used, and the challenge is to encourage greater uptake of these approaches. In the case of conserving rare plants that depend on the crop, we are much further away from converting new knowledge into management practices for nature conservation. Overall, however, it is clear from the evidence we provide that facilitative plant interactions can play a central role in making crop systems more sustainable.

Image caption: Harvesting a study of the impact of barley mixtures on rare and common weed species.
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 should the number of leaves along branches in a plant canopy change with leaf size?

Yingxin Huang, Martin J. Lechowicz, Charles A. Price, Lei Li, Ying Wang and Daowei ZhouSongnen Grassland. Photo provided by authors.

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The three dimensional array of leaves and branches that comprise a plant canopy functions primarily as an integrated system for the capture of solar energy and the uptake of carbon dioxide in photosynthesis. The placement of leaves along branches, influenced by both leaf size and number, affects the whole plant architecture and resource economics in numerous ways. If a species has large leaves, they must be spaced farther apart to avoid self-shading. Conversely, a species with small leaves can pack more leaves onto a branch before self-shading is an issue. Given two species differing in the size of their leaves, can we predict how many leaves they will have relative to the amount of branch – their leafing intensity?

Working from established principles, we show algebraically that the relationship between leaf size and leafing intensity depends on the density of branch tissues. The allocation of biomass to leaves versus branches interacts with the density of branch tissue to determine the size and number of leaves on branches within a given volume of a plant canopy. When the relative biomass investments in leaves vs branch tissues as well as the density of branch tissues are constant, then leafing intensity will differ in simple inverse proportion to leaf size. That is, a species with leaves 10% bigger than another species will have a 10% smaller leafing intensity. Conversely, any change in the density of branch tissue will affect the relationship between leaf size and leafing intensity. Leafing intensity will still be smaller in the species with bigger leaves, but the leafing intensity will not diminish proportionately to changes in leaf size. We affirmed these predictions in comparisons of wildflowers growing in the Songnen Grasslands of northwestern China. These results emphasize the importance of considering the complex tradeoffs among traits that influence adaptive evolution of the structure of plant canopies.

Image caption: Songnen Grassland. 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.

 

The effects of background risk on behavioural lateralization in a coral reef fish

Maud C.O. Ferrari, Mark I. McCormick, Bridie J. M. Allan, Rebecca B. Choi, Ryan Ramasamy and Douglas P. ChiversImage provided by authors.

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Many animals show an asymmetry (or lateralization) in their organ use, much like human handedness. For instance, some birds use only their left eyes to recognize environmental cues used during migration. Given that numerous studies have reported many benefits associated with this asymmetry, it is somehow surprising to see the variability in the degree of lateralization within and across populations, species and taxa. A few studies have reported changes in the degree of lateralization of individuals, in response to long-term changes in environmental conditions. However, we do not know if short-term changes in conditions could change the degree of lateralization displayed by an individual. Predation is highly variable over both space and time. Thus, predation risk is a potential factor that could induce such changes.

Here, we exposed wild-caught juvenile damselfish to a high or low background level of risk for four days and showed that the fish subsequently differ in their turning bias. Fish from the low-risk environment did not display a strong turning preference, while fish from a high-risk background showed a strong turning bias (turning more consistently right or consistently left), a trait previously linked to increased chance of escape during predator attacks. Fish from the high-risk background also had higher survival when released into experimental environments containing reef predators. This demonstrates that lateralization, traditionally thought of as a fixed trait, is rather flexible. More work is needed to investigate the mechanism underlying this plasticity.

Image caption: 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.

 

Leaf traits of vascular epiphytes shift with height above the forest floor

Gunnar Petter, Katrin Wagner, Wolfgang Wanek, Eduardo Javier Sánchez Delgado, Gerhard Zotz, Juliano Sarmento Cabral, Holger KreftResearch crane at the San Lorenzo Canopy Crane Site in Panama (left). Prosthechea sp. (Orchidaceae) in flower; leaves of Serpocaulon wagneri (Polypodiaceae) and Stenospermation angustifolium (Araceae; right, from top to bottom). (Photos by G. Petter).

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Leaves control the water and carbon balance of plants. Leaf traits can thus strongly influence growth and survival of plants under different environmental conditions. In dry areas, for instance, plants with thick and leathery leaves are often more successful, illustrating a linkage between leaf traits and the environment. Environmental gradients offer great opportunities to study how environmental conditions affect leaf traits, and which traits are functionally important. Within forests, environmental conditions change gradually with height above the forest floor, from the dark and humid understory to the sunnier and drier outer canopy. Vascular epiphytes, which are plants growing non-parasitically on trees, are exposed to all these different conditions, making them particularly useful for studying how such vertical gradients affect the vertical distribution of leaf traits within and across species. A few studies have compared epiphyte traits at different heights or different positions within trees, but none so far has systematically examined changes in leaf traits along the entire height gradient.

In this study, we analyzed the relationship between several leaf traits of epiphytes and height in a Panamanian lowland rainforest. We accessed the canopy with a research crane. For most traits, the average trait value changed with height, but the pattern of change differed between traits. For instance, while the average leaf thickness increased gradually with height, the average specific leaf area (leaf area/leaf dry mass) decreased strongly only in the first meters above the forest floor. Such trends were similar within the major taxonomic groups of epiphytes (orchids, ferns, bromeliads, aroids), but mean trait values between these groups sometimes differed substantially. Interestingly, trait shifts were also observed within species, indicating that individuals of the same species can respond to environmental changes even over only a few meters of height. We also found that species with higher leaf trait variability occurred at a greater range of heights within the forest. In summary, we observed a link between leaf traits and the vertical environmental gradient within forests at community and species level, contributing to our understanding of the vertical distribution and trait composition of epiphyte communities.

Image caption: Research crane at the San Lorenzo Canopy Crane Site in Panama (left). Prosthechea sp. (Orchidaceae) in flower; leaves of Serpocaulon wagneri (Polypodiaceae) and Stenospermation angustifolium (Araceae; right, from top to bottom). (Photos by G. Petter).
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.

Review

Plants respond to herbivory by producing more prickles, thorns, and spines

Kasey E. Barton Hawaiian prickly poppy. Photo provided by author.

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Anti-herbivore plant defense is highly variable, changing within plants as they grow, and in response to their environments. Induced defenses occur when plants respond to herbivory by increasing defense traits. While considerable research has examined how plant defensive chemistry changes after herbivory, often leading to more poisonous and better defended plants, relatively little is known about herbivore-induced changes in physical defenses.

Plant physical defense traits include external structures that deter herbivores such as hairs, spines, thorns, and prickles, as well as internal cellular structures, such as calcium oxalate crystals and lignin, that make leaves tough to digest. Like defensive chemicals, physical defense traits may increase following herbivory, making plants better defended against future attacks. However, because induction of physical defense traits requires the growth of new tissues (with more prickles or tougher leaves), it is slower than chemical induction, leading scientists to predict that physical trait induction is likely to be less common and of lower magnitude than chemical induction.

In this study, we performed a meta-analysis to examine general patterns in the induction of physical defense traits. All studies that have been published on physical trait induction were identified, and the data for defense traits in undamaged control vs. damaged treatment groups were extracted and analyzed together.

The results reveal that physical trait induction is common and widespread. In contrast to the prediction, the magnitude of physical trait induction (52%) was not lower than chemical trait induction (43%), and was actually slightly higher. Interestingly, not all physical defense traits are inducible to the same degree. Non-glandular hairs showed the greatest induction (mean 82%), while prickles (40%), spines (26%) and thorns (54%) showed weaker, but still significant increases. Leaf toughness did not respond to damage, perhaps because leaf toughness is more important for eco-physiological functions.

This research highlights some general patterns in plant induced responses to herbivory. However, it also reveals important gaps in our knowledge. For example, very few studies actually examine whether the induction of more prickles, thorns, and spines actually improve defense against future attacks. Therefore, the ecological and evolutionary significance of these responses remain unclear.

Image caption: Hawaiian prickly poppy. Photo provided by author.
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.

 

Evolution of nutrient acquisition: when space matters

Sébastien Barot, Stefan Bornhofen, Simon Boudsocq, Xavier Raynaud and Nicolas Loeuille Grass layer of the savanna in Hwange National Park, Zimbabwe. Photo provided by authors.

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Ecologists have extensively studied plant strategies (sets of characteristics that allow plants to survive and reproduce in particular environments), and a key characteristic of these strategies is the rate at which plants acquire mineral nutrients from soils. This rate should not only strongly influence the success of plant species confronted by competition for resources, but should also have an impact on ecosystem characteristics such as the availability of mineral nutrients or primary production. Meanwhile, evolutionary ecology has paid little attention to the evolution of traits, such as the rate of nutrient uptake, that affect fitness (measured as the number of descendants) only indirectly but are closely linked to ecosystem functioning. Using a theoretical approach, we therefore studied the evolution of the rate of nutrient uptake and the consequences of this evolution for ecosystem characteristics. We built a spatially-explicit simulation model where a limiting nutrient is recycled in local patches by individual plants. The model includes both local competition for the local nutrient source in each patch and regional competition for the colonization of all patches. We show that heterogeneity in nutrient availability and limited capacity to disperse seeds mitigate the effect of competition for the local nutrient resource and allow the evolution of lower rates of nutrient uptake. Our spatially explicit model suggests that evolution in richer ecosystems selects "expensive" strategies (high acquisition, but low conservation of resources) compared to poor ecosystems. Low rates of nutrient acquisition can be considered as a form of altruism because they leave more resource available for other individuals. Our model thus suggests that the influence of spatial processes on the evolution of altruism is pervasive and is linked to key aspects of ecosystem functioning. Our work confirms that the interplay between local and regional competition is critical for the evolution of plant nutrient strategies and its effect on ecosystem properties. Our approach could be used to study the evolution of many traits allowing plants to control nutrient availability, e.g. the capacity to control the mineralization of dead organic matter or nitrification. This should be particularly important in the context of global changes because plant reactions to these changes are both ecological and evolutionary.

Image caption: Grass layer of the savanna in Hwange National Park, Zimbabwe. 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.

 

Defenders in the Tundra: Plant defense is determined by nutrient availability and elevation

Jonathan R. De Long, Maja K. Sundqvist, Michael J. Gundale, Reiner Giesler and David A. Wardle Photo credit: Paul Kardol.

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Plants use chemical and structural defense compounds to protect themselves from herbivory and harsh environmental conditions. Many of these compounds also influence decomposition rates in dead leaves and thereby control nutrient cycling and availability. A number of theories predict that alleviating nutrient limitation in the soil, namely nitrogen (N) and phosphorus (P), and reducing other environmental stressors such as harsh climatic conditions, will result in decreased production of plant chemical defenses. Basically, plants will need reduced defense against herbivory and environmental stresses when growing conditions are more favorable. In this study, we measured plant defense properties in both fresh and dead plant leaves in a N and P fertilization experiment set up at each of three elevations in Swedish subarctic tundra heath vegetation. We also measured how responses of defense properties at the plant community level to elevation and nutrient addition were driven by variation within species (i.e., different members of the same species) versus variation among species. We hypothesized that N fertilization would reduce plant defense properties and that this reduction would be greater at higher elevations where nutrients are most limited and climatic conditions are least favorable, while the effects of P fertilization would have no effect at any elevation. Broadly in line with our hypotheses, N fertilization reduced most plant defense compounds in both fresh and dead leaves, while P fertilization had few effects. The effects of N fertilization frequently varied with elevation, but in contrast to our hypothesis, these effects were strongest at the lowest (i.e., warmest) elevation. The effect of N fertilization and its interactive effect with elevation were primarily driven by variation within species, rather than by variation between different species. Our findings suggest that as temperatures warm and N availability increases due to global climate change, defense compounds in subarctic heath vegetation will decline particularly within species. These results highlight the need to consider the effects of both nutrient availability and temperature, and their interaction, in driving subarctic plant defense.

Image caption: Photo credit: Paul Kardol.
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.

 

Parent-offspring co-adaptation in a wild bird

Carsten Lucass, Peter Korsten, Marcel Eens, Wendt MüllerBlue tit brood. Photo credit: Wendt Müller.

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The offspring of many animals depend on their parents’ care (like the provision of food) and have to solicit such care through specific behaviours such as begging, as exhibited by hungry nestlings in birds. Nestlings beg more intensely when they are hungrier, to stimulate their parents to bring more food. When the parents do so, the offspring thus become less hungry and so beg less in turn. Because of the tight interplay between parents and offspring, their behaviours will evolve in order to adapt to each other, leading to ‘co-adaptation’ between parents and offspring. Because behaviours are flexible and parents and offspring continuously respond to each other, it is unlikely that the overall levels of begging and food provisioning are co-adapted; it is more likely that the amounts of change in both the offspring’s begging when they become hungrier and the parents’ provisioning in response to this begging will be co-adapted. Thus, the behavioural responses of parents and offspring may be matched within families. For example, parents that are relatively unresponsive to their offspring’s begging may be better matched with very responsive offspring, because highly responsive parents would overload such responsive offspring with food, rapidly tiring themselves. To test this, we studied wild blue tits. We exchanged same-sized clutches between breeding pairs to disrupt the behavioural match between parents and their offspring. Next, we measured the provisioning responses of parents to changes in food demand of their foster brood (by temporally manipulating their brood size) and the begging responses of the nestlings in relation to different hunger levels. We found the mother’s provisioning and genetic offspring begging were unrelated. However, even though fathers were not raising their own offspring, the provisioning and begging responses of fathers and their genetic offspring (raised by foster parents) were related. Fathers that strongly respond to changes in brood demand have genetic offspring that only show weak begging responses when hungry and vice versa. This is the first study to show the evolutionary interplay between behavioural responses of both parents and offspring. The outcomes are highly relevant for improving theoretical models of parent-offspring co-adaptation.

Image caption: Blue tit brood. Photo credit: Wendt Müller.
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 relationship between microhabitat use, allometry, and functional variation in the eyes of Hawaiian Megalagrion damselflies

Jeffrey Scales & Marguerite ButlerThe eyes of  Megalagrion n. nigrolineatum, an example of a Hawaiian damselfly that breeds along pools.

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The eyes are our “windows to the world”, but do they match where we live? One of the ways in which animals generate biodiversity is through the process of adaptation, for example when the beaks of birds matches the food type they specialize on. The eyes, while not as well-studied for ecological adaptation as the jaws for feeding or limbs for locomotoion, are particularly interesting because eyes are under a lot of constraints. Fundamentally, larger eyes can see better because larger eyes with larger photoreceptors can collect more light. To produce a finer image, however, requires more photoreceptors viewing the same image. Nowhere are these constraints more obvious than in the eyes of insects, with their modular organization. How this tradeoff is resolved, and how it interacts with size is a very interesting question for visual evolution, and is especially apparent in forest-dwelling flying insects, where the habitat may be dark and variably lit, and insects face additional constraints related to flight. Here we examine how differences in size and habitat use (where they live within the forest) influence the visual design of the eyes of closely related Hawaiian damselflies. While all of the Hawaiian damselflies rely heavily on vision to capture prey and find mates, they live in slightly different habitats within the forest that differ in lighting and complexity. We find that eye size is tightly linked to body size so that larger damselflies have larger eyes. However, other eye traits related to light sensitivity and visual resolution are associated with the “niches” used by damselflies. Because eye design varies with small differences in habitat, species with small eyes should be able to see as well, or better than even the largest Hawaiian damselfly species. Thus, even small species with relatively small eyes can live in dark habitats. These findings suggest that although body size plays an important role in determining eye size, eyes can be fine-tuned to match their different microhabitats, and there is sufficient variation to exploit even small scale differences.

Image caption: The eyes of Megalagrion n. nigrolineatum, an example of a Hawaiian damselfly that breeds along pools.
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.

 

Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context, and reproductive state

Glenn T. Crossin, Oliver P. Love, Steven J. Cooke, & Tony D. WilliamsResearchers prepare an adult Atlantic salmon (Salmo salar) for physiological manipulation in order to test predictions regarding individual variation in overwinter migration strategy. Photo by Xavier Bordeleau.

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Attempts to identify the physiological basis of life-history variation in wild animals often use an experimental increase or blocking of a particular hormone combined with observations of subsequent behaviour, breeding investment (e.g. fecundity, parental care), and survival. Experimental manipulations of ‘stress’ hormones (glucocorticoids - GC) can be very useful, but predicting their effects is often difficult. Much uncertainty can emerge given that GCs possess a dichotomous physiological role: baseline levels regulate daily energy use while higher levels mediate responses to stress. As such, the relative levels that are expressed and their interaction with life stage, ecological variation, age, and sex can differentially impact fitness.

In this Perspectives piece, we review the literature surrounding GC manipulations, discuss the potential pitfalls when designing GC studies, and make recommendations for how future studies can benefit by considering broader sets of overarching hypotheses. Ultimately, we urge researchers to consider three key points when designing experiments: the life-history context of the species under study (e.g. long- vs. short-lived, reproducing only once or repeatedly, etc.), the ecological context that it is studied in, and the choice of the most appropriate GC dose that will best test the predictions posed by the hypotheses.

Image caption: Researchers prepare an adult Atlantic salmon (Salmo salar) for physiological manipulation in order to test predictions regarding individual variation in overwinter migration strategy. Photo by Xavier Bordeleau.
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.

 

Evidence of trophic specialization in cave species challenges the usual prediction of generalist feeding in food-limited environments

Clémentine Francois, Florian Mermillod-Blondin, Florian Malard, Francois Fourel, Christophe Lécuyer, Christophe J. Douady and Laurent SimonSampling of groundwater organisms at Borne aux Cassots cave (France). Photo: Robert Le Pennec.

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The identification of feeding strategies along a specialist-generalist continuum is fundamental to the understanding of many ecological processes associated with food web structures and ecosystem functioning. Theory states that the amount of food available in a given environment influences these feeding strategies. In food-limited environments, generalist species are expected to occur because species may not be able to subsist when feeding only on a reduced set of food sources. However, species living in these poor environments often exhibit peculiar biological traits, such as improved food-finding abilities or low metabolic rates, which may release the constraints due to low food availability, and allow for specialist species even in these harsh habitats.

This paper tested this hypothesis of specialist species in food-limited habitats by focusing on two aquatic cave-dwelling water slaters (isopods within the Proasellus genus), as they live in one of the most food-limited environments on Earth. We used carbon and nitrogen stable isotopes (13C and 15N) to quantify the transfers of carbon and nitrogen from each food source to the organism.

The degree of specialization of these two isopod species was determined in the laboratory by measuring the rate at which they assimilated C and N when being fed separately with one of the 3 food sources available in caves: fine and coarse particulate organic matter (corresponding to fragments of leaves and wood of different sizes) and sedimentary biofilm (corresponding to the conglomeration of microorganisms developed on the surface of sediments). We demonstrated that both species assimilated far more (up to 10 times) C and N from the sedimentary biofilm than from both kinds of particulate organic matter, indicating a high degree of specialization on biofilm.

In parallel, the actual diets of these isopods were estimated for five populations (= five distinct caves) per species. All isopods fed predominantly on the sedimentary biofilm (representing in average 83 % of the diet), regardless of the population or species considered.

Our results showed for the first time in cave species a strong trophic specialization on the sedimentary biofilm. This evidence of specialist species in groundwater challenges the traditional view of the selection of generalist species in food-limited environments.

Image caption: Sampling of groundwater organisms at Borne aux Cassots cave (France). Photo: Robert Le Pennec.
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 does temperature affect colonies of a pollinating bumble bee?

Jacob G. Holland and Andrew F. G. BourkeInside a nest of the buff-tailed bumble bee (Bombus terrestris), complete with marked bees. Photo credit: Andrew Bourke, 2013.

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Many plants are entirely dependent on pollination by insects, but this interaction may be disrupted by predicted future climate change. Since this has the potential to create costly environmental and economic problems, it is vital that we understand how these insect pollinators respond to changes in temperature. A number of important insect pollinators live in complex social colonies, which are fundamental to almost every aspect of their biology, and yet we understand little about how these colonies are affected by temperature. We investigated this relationship using colonies of buff-tailed bumble bees, which are common in the British Isles and the rest of Europe. Bumble bee colonies develop from a single queen, but can reach several hundred individuals before producing new queens and males, which are needed to produce daughter colonies in the following year. When exposing laboratory colonies to two different temperatures (20oC or 25oC), we found that the lifespans (longevities) of individual bees were surprisingly resilient to temperature differences. However, we also found that colonies, when taken as a whole, responded in more complex ways to temperature. For example, higher-temperature colonies produced more queens and lived slightly longer, but did not differ in the timing of their growth. These findings show that it is important to consider the effects on whole colonies when predicting the responses of social bees and other social animals to environmental changes.

Image caption: Inside a nest of the buff-tailed bumble bee (Bombus terrestris), complete with marked bees. Photo credit: Andrew Bourke, 2013.
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.

 

Seed transport by physically active animals: farther than we think?

Casper H.A. van Leeuwen, Rosanne Beukeboom, Bart A. Nolet, Elisabeth S. Bakker, Bart J.A. PolluxCarp in tank. Photo provided by authors.

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Seeds enable plants to spread within and between patches of suitable habitat. Wind and water often transport ripe seeds to new places. However, also animals can be vectors for seeds: many animals feed on nutritious seeds or fruits, but do not completely digest all the ingested food. Numerous plants produce seeds that can still germinate after multiple hours of retention in the digestive system of animals. In case animals defecate these seeds after they have moved to a new location, plants may spread into new suitable habitat.

To estimate the impact of this dispersal mechanism on ecosystems, we need to estimate how far animals might be able to transport seeds. This largely depends on how long it takes before an ingested seed is defecated again. This is often determined experimentally by feeding animals with a known quantity of seeds, followed by monitoring seed retrieval over time. However, up until now, almost all these experiments have been performed with animals resting in cages, while animals dispersing seeds in the wild will be actively moving elsewhere by either swimming, walking or flying. We hypothesized that seed digestion in resting animals would be different than in animals engaged in the physical activity involved in moving to new habitat.

In our study we therefore compared seed retrieval patterns between animals that were resting in a cage, and actively swimming animals. We used common carp as a model species, as fish are increasingly recognized as important seed dispersers in rivers, particularly for plants colonizing upstream habitat. Physically active fish were found to retain ingested seeds for up to two hours longer than resting fish. This implies fish may transport seeds many kilometres further upstream in river systems than previously estimated. We expect that also in other seed dispersing animals physical activity will influence their seed digestion, and emphasize that this should be taken into account when making predictions of the impact of seed dispersal by animals on ecosystems.

Image caption: Carp in tank. 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.

 

What can we predict about a forest based on the sizes of its trees?

Kristina J. Anderson-Teixeira, Jennifer C. McGarvey, Helene C. Muller-Landau, Janice Y. Park, Erika B. Gonzalez-Akre, Amy C. Bennett, Christopher V. So, Norman A. Bourg, Jonathan R. Thompson, Sean M. McMahon & William J. McSheaImage provided by authors.

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Numerous characteristics of trees vary predictably with trunk diameter. These include height and other dimensions, water use, growth rate, mortality rate, and abundance. The mathematical descriptions of these relationships, known as “scaling relationships”, are broadly useful for understanding forests globally and their role in Earth’s changing climate system. Characterizing scaling relationships and understanding the underlying mechanisms are therefore of great value.

This study, which was conducted in a forest at the Smithsonian Conservation Biology Institute, Virginia, characterized scaling relationships for a broad suite of tree characteristics. Field measurements were used to quantify how tree height, crown dimensions, water use, growth rate, mortality rate, and abundance related to trunk diameter. To put results from this forest in a global context, corresponding scaling relationships observed in forests throughout the world were reviewed. All of these results were used to evaluate the consistency of observed scaling patterns in forests with the predictions of ecological theory.

Results show that existing ecological theory had mixed success at predicting scaling patterns in forests. Some tree characteristics, such as height, were relatively well explained by theoretically predicted scaling relationships. However, scaling relationships for some other characteristics, such as growth rate, deviated meaningfully from theoretical predictions, pointing to mechanisms that have not yet been accounted for. Scaling patterns also varied among tree species and were affected by environmental variation. These findings reveal that while existing ecological theory can often provide reasonable approximations of scaling patterns, a more nuanced understanding of scaling in forests will be important to characterize forest structure and function with sufficient precision to address some of the most pressing questions in forest ecology. In particular, a more refined understanding of scaling in forests will be invaluable in the current era of global change, when understanding how forests are changing and interacting with Earth’s climate is important for both forest conservation and climate change mitigation.

Image caption: 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.

 

Big, warm woodlice “chill out”, rather than cross a habitat corridor

Andrew D. Barnes, Ina-Kathrin Spey, Lena Rohde, Ulrich Bros, and Anthony I. Dell Camera system (left) within the environmental chamber used to film woodlice as they move around an experimental fragmented landscape (right, blue line indicates woodlice trajectories), also seen at the bottom of the filming chamber. Woodlice movement patterns can then be automatically tracked and analysed using automated image-based tracking software.

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With increasing global temperatures and habitat fragmentation, the question of whether animals will be able to cope with these environmental changes becomes increasingly important. Species are already tracking rising temperatures by moving to cooler latitudes or elevations in order to remain in their preferred temperature ranges. However, the ability of species to do this is hindered by habitat fragmentation. One possible solution is to create dispersal corridors that link habitat fragments, thus allowing animals to move more easily across the landscape. This gives rise to another important question: will changes in temperature alter the way animals use corridors?

Theory and data suggest that larger and warmer animals should be more active, thus suggesting that larger, warmer animals should encounter habitat corridors more often. To test this, we used novel automated methods to track the movement of different sized woodlice around a fragmented experimental landscape at temperatures ranging from 15 to 25 ºC. By quantifying the movement and behavior of individuals (e.g., mean and maximum body velocity, the proportion of time spent moving, corridor encounter rate), together with overall corridor crossing rates, we were able to isolate the biological mechanisms driving the relationship between body size, temperature, and corridor use.

Surprisingly, our results showed that warmer and larger woodlice moved more slowly and crossed corridors less often than colder and smaller woodlice. We also found that the woodlice which moved more often crossed habitat corridors less than the less active woodlice. We explain these counterintuitive findings by individual variability in behavioural responses to warming. Our results suggest that individual behaviour plays a key role in determining how animals use habitat corridors, making the story more complicated than might be expected from general theory, such as a general metabolic response to rising temperature. Understanding this story becomes more critical as global temperatures continue to rise and landscapes become ever more fragmented.

Image caption: Camera system (left) within the environmental chamber used to film woodlice as they move around an experimental fragmented landscape (right, blue line indicates woodlice trajectories), also seen at the bottom of the filming chamber. Woodlice movement patterns can then be automatically tracked and analysed using automated image-based tracking software.
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.

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