Lay summaries for Volume 31, Issue 3 of Functional Ecology

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FE Spotlight

Handbook of Invertebrate Functional Traits


Plant physiological ecology

Plant-animal interactions Plant-animal interactions

Animal physiological ecology

Behavioural ecology

Evolutionary ecology

Community ecology

Ecosystem ecology

FE Spotlight


Functional trait ecology in the Anthropocene: a standardized framework for terrestrial invertebrates Cleo Bertelsmeier

Handbook of Invertebrate Functional Traits

Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits

Marco Moretti, André T.C. Dias, Francesco de Bello, Florian Altermatt, Steven L. Chown, Francisco M. Azcárate, James R. Bell, Bertrand Fournier, Michael Hedde, Joaquín Hortal, Sébastien Ibanez, Erik Öckinger, José Paulo Sousa, Jacintha Ellers and Matty P. BergPhotographs of Isopoda  by Theodoor Heijerman.

Traits are simply species characters that can be measured or observed directly and are commonly a descriptor of a behavioural or morphological adaptation. The first well known observation was made by Charles Darwin who famously described the shape of finch bills and their functional relationship with seed size and form. Beyond shape and form, traits strike at the very heart of how individuals increase their survival and fitness in relation to environmental conditions - Darwin’s theory of natural selection brilliantly illustrated that. Relating traits to functions can ultimately provide a measure of how key ecosystem processes and services, like nutrient cycling and pollination, might be affected if communities were to change. Perhaps not surprisingly, the practical side of trait ecology is little different to how taxonomists collect measurements to describe new species: ecologists collect measurements like body size, life span, eye morphology and these are then mapped using a standardized protocol. Measurements are projected in a ‘trait space’ that displays the range and variability of traits of interest, and in doing so, seemingly unrelated species are linked to identify general principles and emergent ideas. Traits have yet to realize their full potential because the methodology is rarely standardized outside of plant ecology, an issue that we try to resolve in this paper for terrestrial invertebrates. We propose the first handbook of protocols for standardized measurements of 29 terrestrial invertebrate traits known to be sensitive to global stressors and to affect key ecosystem processes and services. As has been the case with plants, standardized functional traits will be used in the future to explain invertebrate community assembly, species diversity patterns, and ecosystem processes and services within and across taxa and trophic levels. Meta-analyses across regions and ecosystems will likely highlight future weaknesses and vulnerabilities in communities, as they have done to some extent with pollination. Importantly, we have left room for new knowledge to be incorporated into the trait protocols, using a standard format within which researchers can further provide methodological input for additional special cases.

Image caption: Photographs of Isopoda by Theodoor Heijerman.
Read the article in full here.


Does biomass-growth increase in the largest trees? Flaws, fallacies and alternative analyses.

Douglas Sheil, Chris Eastaugh, Mart Vlam, Pieter Zuidema, Peter Groenendijk, Peter van der Sleen, Alex Jay and Jerome VanclayImage provided by authors.

Trees play a major role in the global carbon cycle and our understanding of tree growth informs forest science and management. Yet the characteristic growth pattern of most tree species remains unknown. Until recently most researchers thought that biomass-growth declined at large stem sizes. But recent studies claim to show that biomass-growth increases throughout a tree’s life with no ultimate decline both in forests and in open-grown competition-free environments. Such contrasting views merit careful assessment. Here we examine how methodological issues can influence the detection and interpretation of biomass-growth trends.

Growth studies of large trees pose various challenges. These challenges range from finding enough of such trees (they typically occur at low densities) to measuring them in an accurate and consistent manner (see figure). Correcting stem measurement errors can itself cause biases that increase perceived biomass-growth with tree size. To estimate biomass change from tree measurements requires the size-biomass relationship to be well characterised (calibrated) but for most species and for large stems in general, these relationships remain unknown. Using general species-averaged size-biomass relationships leads to large uncertainties regarding biomass and biomass-growth at large sizes in each species. A problem arises when growth patterns within and among stems are confused (these patterns can be distinct as they reflect distinct ecological processes).

To explore and illustrate some of our concerns we use growth-rings to examine the lifetime growth of 14 tropical tree species. Our examination of estimated biomass-growth in 706 stems indicates similar numbers of positive and negative trends with most trees having relatively flat growth (i.e., without marked trends) over extended periods. Nonetheless, when we compare stems all but one of our 14 species indicate higher biomass-growth in the larger stems. Individual stems and patterns across stems thus lead to contrasting conclusions: any confusion of these would constitute a so called “Ecological Fallacy”.

We note that recent studies concluding that biomass-growth increases as stems grow larger do not in fact examine patterns in individual stems but compare variation in growth among stems. Patterns among stems themselves remain uncertain too, due to errors and possible artefacts. We describe how these problems can be avoided or reduced so as to provide reliable results and conclusions.

Image caption: Image provided by authors.
Read the article in full here.

Plant physiological ecology

Wood anatomy reflects different ecological strategies in tropical rainforest lifeforms

Deborah M.G. Apgaua, David Y.P. Tng, Lucas A. Cernusak, Alexander W. Cheesman, Rubens M. Santos, Will J. Edwards and Susan G.W. LauranceAnatomy of a rainforest liana Strychnos minor showing large and largely solitary vessels. Image provided by the authors.

Tropical rainforests harbour a large portion of the world’s plant diversity, yet many scientists fear these communities are at risk from increasing drought events. In order to understand how forests with thousands of species will respond to droughts, we explored how plants that live in different parts of the forest differ in form and function.

We studied 90 plant species in a lowland rainforest in northeast Australia that differed in their habitat preferences, ranging from the dark understorey to the tops of trees. These species formed six ecological groups: mature-phase trees, understorey trees, pioneer trees, understorey shrubs, pioneer shrubs and vines. We sampled wood from these species to collect data on anatomical features related to water transport, such as vessel sizes, frequency and distribution. We also collected leaves from each species to quantify leaf intrinsic water use efficiency through carbon isotope ratios, a measure of how much carbon could be taken up by photosynthesis for a given amount of water lost to transpiration.

Across our study species, we found a spectrum of different wood characteristics. Large climbing plants called lianas, for instance, had low wood densities and exhibited large solitary vessels, indicating an ecological strategy that maximizes water transport at the expense of mechanical support. At the other end of the spectrum, understorey shrubs and trees had high wood densities and numerous small vessels, possibly reflecting a higher investment in structural support, and the reduced need for high water transport. Vessel size was also a strong predictor of water use efficiency across our 90 study species, indicating that plants with larger vessels, and thus a higher potential for water transport, are able to fix more carbon per unit of water transpired. We therefore provide a framework for understanding plant performance through wood functional anatomy and a plant functional group approach.

Image caption: Anatomy of a rainforest liana Strychnos minor showing large and largely solitary vessels. Image provided by the authors.
Read the article in full here.


Climate and tree vigour control the timing of wood formation in deciduous oaks

Gonzalo Pérez-de-Lis, José Miguel Olano, Vicente Rozas, Sergio Rossi, Rosa Ana Vázquez-Ruiz and Ignacio García-GonzálezTransverse section of wood from pedunculate oak (Quercus robur). Dividing cells in the cambial zone (centre) give rise to new phloem (top) and xylem (bottom) tissues.

Trees produce new wood during their whole lifespan. Tissue known as ‘vascular cambium’ generates a new tree ring that is disposed over the existing wood tissues every year. To sustain the machinery of growth, trees need to invest large amounts of carbohydrates produced in the leaves via photosynthesis. Trees adjust how they function in different climates by shifting the timing of growth (i.e. phenology), although this can influence the capability of trees to produce wood. Understanding how phenology affects wood production is of special relevance in the context of climate warming, which is modifying phenological patterns in terrestrial plants.

We monitored wood and leaf formation, and the content of non-structural carbohydrates (NSC), in the stems of two deciduous species, pedunculate oak (Quercus robur) and Pyrenean oak (Quercus pyrenaica), in three sites located along a humidity gradient in northwestern Spain. Although Pyrenean oak is better adapted to drought than pedunculate oak, both species coexist along the transition between the temperate and Mediterranean regions. We also assessed the impact of the number of cambial cells in winter (higher in more vigorous trees) on wood production and phenology during the following growing season.

Pedunculate oak was more productive and had a longer growing season than Pyrenean oak, but both species showed comparable seasonal changes in growth activity and carbon reserves. We show that, under warm and dry conditions, deciduous oaks reduce or even stop growth in summer, but extend the growing season in spring and autumn. Stem NSC dropped in spring simultaneously with the onset of growth, and recovered in summer after the formation of new leaves. Trees with more cambial cells in winter had a longer growing season and produced more wood. This result indicates that tree vigour acts as a predisposing factor for growth, modulating carbon demands throughout the year.

Image caption: Transverse section of wood from pedunculate oak (Quercus robur). Dividing cells in the cambial zone (centre) give rise to new phloem (top) and xylem (bottom) tissues.
Read the article in full here.


Intraspecific trait variation across multiple scales: the leaf economics spectrum in coffee

Adam Martin, Bruno Rapidel, Olivier Roupsard, Karel Van den Meersche, Elias de Melo Virginio Filho, Mirna Barrios and Marney Isaac Photograph provided by authors.

Ecologists are interested in knowing how changes in biodiversity affect ecosystems. Specifically, they are often interested in understanding how biodiversity losses reduce the “services” that ecosystems provide. In agricultural systems for example, we are interested in knowing how reduced diversity affects crop yield, pest outbreaks, or crop responses to climate change. For a long time, ecologists have measured biodiversity simply as the number of species in an ecosystem. But more recently they are interested in “functional diversity”: in other words, the range of leaf, root and stem types that are present in an ecosystem.

Generally, functional diversity is a better predictor of ecosystem services than simply the number of species, so it has become important to know which are the most ecologically important functional traits in plants. Leaf functional traits – notably, photosynthetic rates, the amount of nitrogen in a leaf, and leaf mass per area – get the most attention. One main way ecologists have come to know these traits are ecologically important is by examining how they relate to one another. Looking at the leaves of hundreds of species, they have uncovered general trends in plants globally: as leaf nitrogen goes up, photosynthesis goes up, and leaf mass per area goes down.

While we know this happens across plant species in natural ecosystems (or “wild” plants), we are still unsure i) if these relationships occur when we look across different individuals of the same species, or ii) if these relationships in wild plants also occur in crops, which have been domesticated over many years.

We looked at these questions in coffee, one of the world’s most common (and well-loved) crops. We found that the same leaf traits that are ecologically important in wild plants are also ecologically important in coffee. Specifically, we found that across nearly 400 leaves from 100 coffee plants, as leaf nitrogen goes up, photosynthesis goes up, and leaf mass per area goes down. But in coffee, these relationships are not the same as in wild plants, possibly because coffee has been bred to have a lot of caffeine, much of which may be in leaves.

Image caption: Photograph provided by authors.
Read the article in full here.

Plant-animal interactions

Consequences of a nectar yeast for pollinator preference and performance

Robert N. Schaeffer, Yu Zhu Mei, Jonathan Andicoechea, Jessamyn S. Manson, and Rebecca E. IrwinBumblebees. Image provided by authors.

Pollinators provide essential services in natural and agricultural systems, driving global floral diversity and a significant percentage of food production. At the heart of interactions between plants and pollinators are key floral resources, such as nectar, produced by plants as a reward in exchange for pollination services provided. Comprised mostly of sugars and amino acids, this nectar reward can vary considerably in quality, and pollinator foraging decisions are frequently driven by nectar quality. Recently, considerable attention has been paid to the fact that microorganisms such as yeasts and bacteria often colonize nectar. These microorganisms consume nectar sugars and amino acids, altering the nutritional quality of this key resource. The consequences of these changes for pollinator foraging preferences and reproduction are poorly understood.

Here, we demonstrate that microorganisms in nectar, in particular the yeast Metschnikowia reukaufii, can significantly affect pollinator foraging decisions. Through a series of behavior experiments, we show that the yeast M. reukaufii may act as an honest signal, indicating the availability of nectar to common eastern bumble bee Bombus impatiens workers. Both naïve foragers, with no previous exposure to yeasts, as well as foragers trained to associate yeast with a flower color, used cues associated with yeast to make foraging decisions, actively seeking out yeast-inoculated flowers. However, miniature bumble bee colonies that consumed nectar containing active yeast or dead yeast did not differ in their reproductive performance, even when given a protein-limited diet, suggesting no apparent benefits or costs of yeast for bumble bee fitness.

Taken together, our results suggest that nectar yeasts can enhance floral signaling as well as alter foraging behavior at individual flowers, though these microorganisms may have no direct effect on pollinator performance. Thus, nectar yeasts may play a significant role in mediating pollinator foraging behavior, with consequences for plant fitness and evolution of floral traits.

Image caption: Bumblebees. Image provided by authors.
Read the article in full here.


Competing for seed dispersal: evidence for the role of avian seed hoarders in mediating apparent predation among oaks

Mario Pesendorfer and Walter KoenigA western scrub-jay (Aphelocoma californica) searches the branches of a valley oak (Quercus lobata) for acorns at the Hastings Natural History Reservation in Carmel Valley, California. Photo credit: Jenna Kohles.

Species interactions come in many shapes and forms, from predation to mutualisms. Indirect interactions, mediated by a third party, often occur when two or more species share the same generalist predator. When the predators are also seed dispersers, as is the case for many large-seeded trees whose seeds are harvested by seed-hoarding animals, such indirect interactions can shift from seed dispersal mutualism to predation, depending on the relative seed production of the trees that co-occur in a community. Because the shift of mutualistic interactions from one tree species to another results in increased relative predation of the less-dispersed species’ seeds, this indirect effect is termed “apparent predation” – one tree species indirectly preys on the seeds of another.

To investigate the mechanisms underlying apparent predation, we studied the seed predation and dispersal dynamics of valley oaks (Quercus lobata) at Hastings Natural History Reservation in central coastal California, where they mainly co-occur with two other oak species, California blue oak (Q. douglasii) and coast live oak (Q. agrifolia). In the first year of the study, western scrub-jays (Aphelocoma californica), high-quality seed dispersers that scatter seeds across the landscape by hiding them in the ground, attended Q. lobata trees in large numbers to hoard acorns. However, when attending the trees, the jays encountered lots of aggression from another bird species, acorn woodpeckers (Melanerpes formicivorus) that mainly hoard acorns by storing them in so-called granary trees. These low-quality dispersers only help the oaks when they accidentally drop an acorn during transport and thus mainly function as seed predators.

In the second year of the study, Q. lobata and Q. agrifolia acorn crops were similar to the first year, but Q. douglasii crops increased tenfold. With acorns more widely available across the landscape, western scrub-jays only attended Q. lobata trees sparsely, likely to reduce the risk of injury during encounters with the woodpeckers which vigorously defend their preferred valley oaks in year-round territories. The jays have much larger home ranges in the fall and were able to optimise their foraging behaviour by shifting to less-preferred Q. douglasii acorns. As a result, Q. lobata trees experienced a proportional increase in seed predation and almost no seed dispersal from jays. Q. douglasii thus exerted apparent predation on Q. lobata acorns.

Indirect effects mediated by shared seed predators and dispersers may be one of the mechanisms that allows for the co-existence of multiple oak species in forest communities. The variable seed production of each tree species appears to drive seed predation and dispersal dynamics in ways previously not explored. Follow-up studies are necessary to investigate the details of the spatial and temporal variation of such species interactions in order to tease apart the fitness consequences for all the members of the community.

Image caption: A western scrub-jay (Aphelocoma californica) searches the branches of a valley oak (Quercus lobata) for acorns at the Hastings Natural History Reservation in Carmel Valley, California. Photo credit: Jenna Kohles.
Read the article in full here.


Aphid-generated indirect interaction network

Yoshino Ando, Shunsuke Utsumi and Takayuki OhgushiFigure showing how aphid created an interaction network through ant-mediated and plant-mediated indirect effects.

A wide variety of herbivorous insects may share a host plant. Since the strength and direction of an interaction between two species can be indirectly altered by a third species, multiple insect herbivores on plants can interact directly and indirectly with each other.

Herbivory can induce morphological and/or chemical changes in plants, thereby affecting interactions with subsequent insect herbivores, called a plant-mediated indirect effect. Although past studies have focused on interactions between co-occurring species, plant-mediated indirect effects can affect plant-associated arthropod communities by connecting species that are separated in time and space. However, little is known about how and to what extent multiple direct/indirect interactions can create an interaction network through plant-mediated indirect effects.

We focused on the potential role of an aphid in creating an interaction network on tall goldenrods, and used an aphid exclusion experiment to examine how the aphid affects the interaction network through aphid-generated indirect effects and its consequence for plant reproductive success .

The aphid played a critical role as a network creator in determining the interaction network. The aphid indirectly decreased co-occurring insects through their removal by ants (an ant-mediated indirect effect). Also, late in the season when the aphid was no longer present, it still indirectly decreased scale insects but increased grasshoppers through aphid-induced leaf regrowth. As a result, aphid-induced leaf regrowth greatly contributed to an increase in the interaction diversity and complexity by connecting co-occurring and temporally-separated herbivores. Moreover, the aphid-generated interaction network could improve the reproductive success of tall goldenrods by increasing seed production.

Image caption: Figure showing how aphid created an interaction network through ant-mediated and plant-mediated indirect effects.
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.

Animal physiological ecology

How will climate change affect predatory invasive species?

Brian S Cheng, Lisa M Komoroske and Edwin D GrosA predatory Atlantic oyster drill rests upon an Olympia oyster. In many parts of the world, oyster drills have been accidentally introduced and may pose a problem for native oysters. These negative effects may intensify with climate change. Oyster drill egg capsules can also be seen on the right side of the photo. Photo credit: Brian Cheng.

The spread of invasive species has resulted in tremendous economic impacts and losses to biodiversity across the planet. There is concern that climate change may worsen the impacts of invaders, partly because many of these species appear to be more tolerant of changing environmental conditions than their native counterparts. However, most of our knowledge in this area is from alien species that are taxonomically related to or that compete with natives. Invasive predators are among the most disruptive non-native species, yet we know almost nothing of how these animals may respond to climate change. To address this, we examined the physiology of two invasive predators (oyster drills – predatory sea snails) and their native prey (oysters) to understand how these species may respond to warming and extreme flood events. We found that these predators were generally less tolerant of extreme climate change conditions as compared to their prey. However, when animals were exposed to conditions representing near-term warming, predator performance and foraging on prey oysters increased greatly. These observations are supported by previous field measurements that indicate intense predation on oysters at the warmest sites. In addition, both invasive predators exhibited different temperatures of peak performance, suggesting that there is a broad temperature range over which predators will consume prey oysters.

Although extreme events appear to favor prey oysters, near-term warming trends may ultimately reduce their abundance in nature. This is a concern, because wild oysters have experienced declines of up to 88% over the last century due to overfishing and habitat degradation. In response, there are active efforts to conserve and restore oyster populations in many parts of the world. Our work suggests that climate change and the invasion of non-native species may severely hamper the recovery of oysters. Future efforts to assist native oysters should consider attempting to eradicate invasive predators that may benefit from climate change.

Image caption: A predatory Atlantic oyster drill rests upon an Olympia oyster. In many parts of the world, oyster drills have been accidentally introduced and may pose a problem for native oysters. These negative effects may intensify with climate change. Oyster drill egg capsules can also be seen on the right side of the photo. Photo credit: Brian Cheng.
Read the article in full here.


Movement ability of an invasive beetle is related to leg length but not body size nor metabolic rate

Pieter A. Arnold, Phillip Cassey, Craig R. White Red flour beetle moving through wheat flour. Schematic of the maze used to assess movement is inset in the top left. Photo: Pieter Arnold.

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Individuals within a species can vary greatly in their ability to move around and disperse within their environment. This variation in movement ability can often be described by physiological, morphological and behavioural traits that are related to dispersal, but the associations among such traits are not always clear-cut or predictable. Previous studies, including work on the invasive cane toad in Australia, have identified that individuals that are larger and have longer legs relative to their body size are able to move farther and faster than smaller or proportionate individuals. In our study, we used an invasive insect species, the red flour beetle, as a model to investigate how movement characteristics related to morphological and physiological traits. Individual beetles were run through a maze that simulated a complex environment, to assess their movement. We identified that movement ability could be described along an axis; individuals that scored positively on this axis moved at higher speed, travelled longer distances, moved continuously, and reached the edge of the maze quicker. Leg length relative to body size was strongly related to movement ability. That is, beetles with relatively long legs had positive movement ability scores, which we hypothesised was because longer legs allow for longer stride length and therefore a greater movement ability. Surprisingly, body size and metabolic rate (energy expenditure) were unrelated to movement ability. This result suggests that dispersal may be more strongly related to the muscles and structures that directly affect locomotion, rather than body size overall or energy-related traits. It will be important for future studies to consider locomotor morphology as a foundation for studying variation in movement and dispersal, especially when investigating the ecology and evolution of traits in invasive or pest species.

Image caption: Red flour beetle moving through wheat flour. Schematic of the maze used to assess movement is inset in the top left. Photo: Pieter Arnold.
Read the article in full here.


Physiological maturity at a critical life-history transition and flight ability at fledging

Allison Cornell, Kate F. Gibson and Tony D WilliamsA fledgling European starling (Sturnus vuglaris) attempts to take off in flight, photo by A. Cornell.

It’s a dangerous world out there for young birds leaving the nest. When songbirds fledge, they make a permanent transition from the sedentary lifestyle of a nestling to a highly active, free-flying fledgling. Outside the nest they have to look for food, escape from predators, and navigate in their habitat. Reported rates of survival show that nearly half of chicks that make this transition die almost immediately, largely due to predators who mark them as easy prey. It’s no surprise that predators choose to go after these juvenile birds; they’re relatively slow to take off, and have poor flight ability.

We investigated the maturity of fledglings on the day they leave the nest, to measure just how developed these young birds are. Consistent with other studies, we found that the values of somatic traits, such as body size and wing length, were smaller than adults. However, when we measured physiological traits that indicate the body’s ability to transport oxygen, we found more than just low trait values. Our fledglings were highly variable in these traits, indicating that this might be a good way to measure the quality of individuals. When we measured the birds’ flight ability, we found that physiological traits were helpful as predictors of take-off angle and energy produced during flight.

When scientists typically study fledglings, only measurements of body size are taken. Our results show that measuring physiological traits might help us distinguish between low and high quality fledglings, because these traits have high individual variation and help predict flight ability. The physiological traits we measured are relatively easy to obtain, and recording these values could greatly impact the way we understand fledglings. If physiological traits are the mechanism driving fledgling flight ability, then for a juvenile bird, physiological maturity could mean the difference between life and death.

Image caption: A fledgling European starling (Sturnus vuglaris) attempts to take off in flight, photo by A. Cornell.
Read the article in full here.


Bad boys bite, good girls eat their dinner

Alexis Y. Dollion, G. John Measey, Raphaël Cornette, Liza Carne, Krystal A. Tolley, Jessica M. da Silva, Renaud Boistel, Anne-Claire Fabre and Anthony Herrel Image provided by authors.

Cranial morphology is complex and how it evolves remains relatively poorly understood. One of the complicating issues is that the head serves many functions ranging from the protection of the brain and major sensory organs to the control of feeding and drinking, and display and communication. These different functions often impose different and conflicting pressures on the size and shape of the cranium in vertebrates. An additional complicating factor is that the selective factors driving the evolution of cranial shape may differ in males and females. Indeed, whereas in males of many vertebrates, and especially lizards, the head is used in territory defense and male-male combat, this is typically not the case in females. Here we explore these issues in a group of dwarf chameleons from South Africa. We quantify skull, mandible and quadrate shape in 3D using a cross-sectional imaging technique (computed tomography, or CT imaging) and test whether skull shape is related to diet as determined by stomach flushing and maximal bite force capacity. Our results do indeed show strong correlations both between shape and bite force, and between shape and diet. Bite force is also related to diet. However, the observed patterns differ between males and females and suggest that the role of the cranium is not identical in both sexes. Our results shed light on the relevance of sex when relating a lizard’s morphological adaptations to its ecological role, and show the importance of collecting comprehensive data on shape, bite force and diet to unravel the selective pressures that govern the evolution of complex integrated structures such as the skull.

Image caption: Image provided by authors.
Read the article in full here.

Behavioural ecology

Which are the drivers of animal personality: hormone levels or metabolic rates?

Benedikt Holtmann, Malgorzata Lagisz and Shinichi NakagawaColour-ringed dunnock (Prunella modularis) from the Dunedin Botanic Garden, New Zealand. Photo credit Stefanie Grosser.

Animals of the same population often show individual variation in their behaviours, which are consistent over time (i.e. repeatable). For example, some individuals are consistently more active, more explorative or more aggressive than others. While these repeatable behavioural differences, referred to as animal personality, have been described in various species, we still know very little about their underlying mechanisms and how personality differences are maintained. Recent studies in the field of animal personality have proposed that consistent individual differences in hormone levels and/or metabolic rates may be responsible for mediating consistent behavioural differences. Thus, here we investigate the relationship between behavioural and the two proposed physiological traits by testing the hypothesis that physiological traits (hormones vs. metabolism) that mediate consistent individual differences in behaviour exhibit similar or higher time-consistency (i.e. repeatability) compared to behavioural traits.

We systematically reviewed published (and unpublished) data from bird species on the repeatability of hormone levels, metabolic rates and behavioural traits, combining results from all relevant articles. Our analyses revealed that both metabolic rates and behavioural traits were highly repeatable and that repeatability estimates of both traits were of similar magnitude. Conversely, the repeatability of hormone levels was three times lower, suggesting that individual hormone levels are more variable over time. These results indicate that individual differences in metabolic rates, rather than hormone levels, are likely a key mechanism involved in generating consistent individual differences in behaviour.

Moreover, additional analyses revealed three more notable findings. First, repeatability estimates of hormone levels and behavioural traits decrease with increasing interval time between two consecutive measurements. Second, males and females differ in repeatability for behavioural traits. And third, hormone level measurements, taken within a few minutes after the capture of an individual (baseline levels) show higher variation than hormone levels taken at least 30 minutes after capture (stress-induced levels).

By conducting meta-analyses, we show that metabolic rates are likely one of the mechanisms underlying consistent individual differences in behaviour. Future studies are now needed to investigate the relationship between metabolic rates and personality traits in more detail.


Cannibalism or burial: undertaking behaviour depends on the change of death cues in termites

Qian Sun, Kenneth F. Haynes, Xuguo ZhouA termite worker consuming a dead worker. Taken by Hu Li.

The ability to detect environmental cues is important for animals to exploit resources and defend themselves against predators and disease. Social insects frequently encounter the dead bodies of their nestmates, which may carry pathogens and could cause an outbreak in the colony. Many social insects dispose of the corpses with a stereotypic behaviour named undertaking behaviour. Ants and honeybees remove the corpses from the nest, but termites that feed on a nutritionally imbalanced woody diet could benefit from recycling rather than discarding nutrients from dead nestmates. Therefore, corpses represent both a food resource and a pathogen risk for termites. As corpses decay with time, the reward from feeding declines and the risk of disease increases. The central goal of our study is to determine how termites regulate this trade-off by detecting chemical cues from corpses. We combined behavioural and chemical analyses to address this question using the eastern subterranean termite, Reticulitermes flavipes.

We found that termites cannibalize the corpses if they are freshly killed, but resort to burying them when the corpses are highly decayed. Such a behavioural switch is mediated by the changes of death cues released by the corpses. Immediately after death, corpses release 3-octanol and 3-octanone. The early death volatile cue, consisting of this alcohol possibly in combination with the ketone, attracts workers to quickly retrieve and consume the bodies, but the two compounds decrease rapidly with time. Correspondingly, there was an accumulation of late death cues, including a blend of phenol and indole, which enable termites to locate the corpses, and a blend of six fatty acids that trigger burial behaviour. Cannibalism is more efficient than burial behaviour, because it requires fewer workers, and also allows termites to recycle nutrients. However, if corpses are not found within the recyclable time frame, burial behaviour could effectively prevent pathogenic propagation.

Our study indicates that the dynamic changes in death cues balance nutritional rewards and infection risks. This post-mortem communication highlights unique adaptations in termites to their feeding habit and social living.

Image caption: A termite worker consuming a dead worker. Taken by Hu Li.
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The price of looking sexy: visual ecology of a three level predator-prey system

David Outomuro, Linus Söderquist, Frank Johansson, Anders Ödeen, and Karin NordströmPhoto provided by authors..

Many animals, such as parrots, tropical fish or butterflies, are very colourful. Such colourful displays are favoured in sexual selection as they make the animal stand out, and colour may therefore enhance mating success. However, colour can also be costly, as it makes the animal more conspicuous to both predators and prey. Colourful traits are therefore subject to opposing selection pressures: positive sexual selection by conspecifics (increased mating success) and negative natural selection by predators (higher predation risk) and prey (lowered hunting success). In this paper we studied the conspicuous wing coloration of two species of damselflies, which are predated by birds and prey on small flies. The conspicuous wing coloration is used in colour communication between the sexes and between different species of damselflies. Using electrophysiology, we first determined the colour vision of the damselflies and found that they see well in UV as well as in the human visible range. Second, we measured the wing coloration using spectrophotometry and confirmed that males are more colourful than females. Third, we estimated the predation risk in natural populations by quantifying the predated wings from bird feeding stations, and found that more males than females were consumed. We finally used our data together with previously known colour vision of the bird predator, and the fruit fly prey, to model how visible the wing coloration is in natural environments. We found that males are very conspicuous to bird predators, to other damselflies, and to prey, while females remain predominantly cryptic (i.e. hard to see against the background). This implies that males, but not females, pay a high cost when they use colour to communicate with other damselflies, both in terms of predation risk and visibility to prey. One of our most surprising findings was that male damselflies are unable to discriminate the wing coloration of perching females! We hypothesize that females use this to reduce male harassment, which is very intense in damselflies. Our study demonstrates that by including several levels of interactions in predator-prey systems, we get a more complete understanding of the costs and benefits of being colourful.

Image caption: Photo provided by authors..
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Evolutionary ecology

A fundamental problem in finding biomarkers confirmed using feather fault bars in nestling birds

Jelle J. Boonekamp, Rutger Dijkstra, Cor Dijkstra, and Simon VerhulstA female jackdaw (Coloeus monedula) approaching her nest box. Photo by Jelle Boonekamp.

Measuring fitness – essentially the product of survival and reproduction - is central to studies in evolutionary ecology that are aimed at gaining an understanding of natural and sexual selection. But measuring real fitness can be difficult and time-consuming, so fitness biomarkers – traits that predict survival and reproduction – are potentially powerful tools in evolutionary ecology when they can be used as surrogate study end points. For example, most vertebrate species have long reproductive lifespans and therefore valuable time and other resources could be saved by using fitness biomarkers.

Useful fitness biomarkers need to fulfil 2 criteria: (i) they need to be accurate predictors of fitness, and (ii) they need to be sensitive to environmental variation (or experimental manipulation), such that the biomarker successfully links environmental conditions to fitness. However, evolutionary theory predicts that traits that are important for fitness should be well protected (canalized) against the influences of environmental fluctuations, and hence biomarkers that are both accurate fitness predictors and sensitive to environmental conditions may be rare.

Here we tested for this canalization principle using free-living jackdaws. We manipulated the number of siblings in the developmental period to test how strongly developmental conditions affected the number of feather fault bars in tail and wing feathers. Fault bars are deformities on bird feathers associated with developmental stress and can cause feather breakage, thereby impairing flight and insulation. We show fault bars in the tail increased when there were more siblings in the nest, while the number of fault bars in wing feathers was not affected, suggesting tail but not wing fault bar number is sensitive to developmental conditions. In line with evolutionary theory, we found that fault bar number on wings, but not tails, predicted fitness prospects. These results confirm the theory that the development of traits that are important for fitness is strongly canalized.

The canalization phenomenon has implications for the utility of traits as fitness biomarkers, because when traits are good fitness proxies, they are also more likely to be strongly canalised, reducing sensitivity to environmental variation. Intriguingly, there are nevertheless traits that are both sensitive to environmental conditions and predict fitness prospects, and we discuss hypotheses that may explain this paradox.

Image caption: A female jackdaw (Coloeus monedula) approaching her nest box. Photo by Jelle Boonekamp.
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The economics of sexual signalling

Thomas M. Houslay, Kirsty F. Houslay, James Rapkin, John Hunt and Luc F. BussièreCrickets.

Sexual selection theory explains the evolution of exaggerated and flamboyant ornaments, displays and mating behaviours in terms of male competition or mating preferences. Such characters are typically costly to produce, but can bring benefits to their bearers: greater mating success for those individuals with the biggest or brightest signals. If an individual produces such signals repeatedly over the course of their adult lifetime, they face ‘trade-offs’ between current and future investment. These trade-offs can create variation in the intensity of signalling at different ages, often interpreted as alternative strategies: ‘live fast, die young’ vs. ‘slow and steady’.

Another possible explanation for this age-related variation is that it is caused by differences in the ability to acquire resources that can be invested in signalling (meaning, for example, that ‘late bloomers’ do not have early investment options). Testing this hypothesis is challenging, not least because measuring both the acquisition and allocation of resources is a difficult task. As an additional complication, an individual’s energetic reserves both affect and are affected by their signalling investment.

Male crickets signal to females using an energetically expensive call, produced by rubbing together their hardened forewings: the more time a male spends calling, the higher his mating success. In this study, we simultaneously manipulated resource acquisition (through diet treatments) and access to females (as a proxy for manipulating sexual signalling) in male decorated crickets (Gryllodes sigillatus). We measured how much time they spent signalling, and how their energy budgets were affected.

Increased diet quality caused increased signalling effort and energy storage, while access to females increased both the likelihood of and time spent signalling. Males with lower resource budgets signalled less, but still suffered energetic losses and reduced lifespan. Our results suggest that energetic constraints, rather than strategic budgeting of resources, led to reduced signalling levels in males with lower acquisition ability. Our findings therefore imply that age-dependent variation in sexual signalling may not represent alternative adaptive strategies. In addition, energetic constraints can help maintain ‘honesty’ in sexual signalling, at least on average: after all, anything spent today cannot be spent tomorrow.

Image caption: Crickets.
Read the article in full here.


Sexual selection in hybridizing lizards

Hannah E A MacGregor, Geoffrey M While, Jade Barrett, Guillem Pérez i de Lanuza, Pau Carazo, Sozos Michaelides & Tobias Uller A typical Italian male from north-central Italy. Photo by Ben Halliwell.

Populations frequently undergo periods of relative isolation and differentiation that are followed by contact and hybridization (interbreeding). What makes hybridization so striking is the many different ways in which it can act as a catalyst for evolution, such as by accelerating the course of speciation or facilitating adaptation through the exchange of genes. But if members of each population look and behave differently then why does hybridization occur at all? Are some individuals more likely to hybridize than others?

Sexual selection has a reputation for preventing hybridization because females commonly prefer to mate with males of similar genes or traits. But in many animals, including many species of lizard, sexual selection via competition among males is the most important cause of mating patterns within populations. Intuitively, in these species male competition should also influence patterns of hybridization when populations come into contact.

Common wall lizards from north-central Italy have highly exaggerated male sexual traits compared to individuals from Western Europe, having diverged in isolation from one another during the last ice-age. Genetic data from a natural contact zone in northern Italy suggests that hybridization may occur asymmetrically, between Italian males and Western European females. In this study, we used experimental contact zones in outdoor enclosures to investigate the consequences of divergence in male sexual traits (such as body size, testes mass, and colour signals) for male-male competition and patterns of hybridization between Italian and Western European lizards.

During our experiment the Italian males completely dominated the Western European males in aggressive encounters, monopolised high quality territory and the courtship of females, and achieved greater reproductive success. Despite our data suggesting a competitive and reproductive advantage of the Italian males with the most exaggerated traits, these superior Italians were not more likely to hybridize. Instead, hybridization between Italian males and Western European females seems to arise because the Italian males with less exaggerated sexual traits are outcompeted for Italian females but remain competitive relative to the Western European males.

Image caption: A typical Italian male from north-central Italy. Photo by Ben Halliwell.
Read the article in full here.


Telomere length and telomerase dynamics in frillneck lizard

Beata Ujvari, Peter A. Biro, Jordan E. Charters, Gregory Brown, Kim Heasman, Christa Beckmann and Thomas MadsenAdult frillneck lizard behind tree.

Much like the plastic tip of shoelaces, telomeres prevent the ends of DNA from fraying during cell divisions. Studies of human cells in culture have shown that telomeres become shorter at every cell division, and when telomeres reach a critically short length (after 50-70 divisions) the cells stop dividing and die. However, many vertebrates produce an enzyme, called telomerase, which replenishes the missing telomere copies. Telomerase not only prevents telomere shortening but is also able to increase the length of critically short telomeres.

In numerous vertebrates, including humans, telomere length (TL) has been shown to decrease with increasing age. Moreover, during recent decades numerous studies have observed an association between TL and organismal survival and/or fitness.

In the present study we therefore investigated how age affected TL and telomerase expression (TE) dynamics in frillneck lizards. We also examined whether TL and TE had any effects on lizard survival. We found that young lizards had short TL, and that TL increased in medium aged lizards but decreased in older cohorts, revealing a curvilinear relationship between TL and lizard age. Higher TE resulted in longer telomeres but in spite of this we did not observe any association between TL dynamics and lizard survival. Instead our results suggest that TL and TE dynamics in frillneck lizards reflect an adaptation to maintain TL above a critical minimum length in order to sustain cellular stability.

Our study has major implications for the role of telomeres in ageing by questioning the significance of TL dynamics as a significant underlying factor in vertebrate survival.

Image caption: Adult frillneck lizard behind tree.
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Community ecology;

Competition shaping the phytoplankton communities, judged from the functional properties of the species

Riina Klais, Veera Norros, Sirpa Lehtinen, Timo Tamminen and Kalle OlliMorphological diversity of phytoplankton, from single cells to different colonies and chains. Photo credit: Dr. Richard Kirby.

Understanding the rules of species coexistence is central for ecological research. Phytoplankton – free-living phototrophic protists and cyanobacteria (the bluegreens) – are known to be controlled by temperature, salinity, light, and nutrients. Species’ environmental preferences define the biogeography and seasonality of phytoplankton functional groups (the most well known being diatoms, dinoflagellates and blue-greens). This knowledge is already used to inform global plankton models. Much less is known about the role of biotic interactions – especially competition – between phytoplankton species in the assembly of natural communities.

We analysed a large coastal phytoplankton dataset, consisting of nearly 8000 samples, collected from the Baltic Sea over the last 30 years, and covering the seasonal cycle and wide salinity and temperature gradients. We first estimated the preferred habitat of every species. From that information, we constructed the simulated communities – as they should be, if only the environment determines community composition. These simulated communities were then compared against the actually observed communities.

We investigated whether the species in the observed community were functionally more or less similar to each other than the simulation predicted. The similarity was judged from characteristics such as body size, ability to fix atmospheric nitrogen, whether they are both auto- and heterotrophic at the same time, whether they swim around, make colonies or chains to change the body shape and avoid predators, and the composition of accessory pigments that phytoplankton use to harvest all the different wavelengths of light that penetrate the water.

When comparing the simulated and observed communities, we found that one in every four communities was notably shaped by competition, because species in it were either too similar, or too dissimilar to each other for their coexistence to be explained only by the environment.

Image caption: Morphological diversity of phytoplankton, from single cells to different colonies and chains. Photo credit: Dr. Richard Kirby.
Read the article in full here.


Integrating intraspecific variation in community ecology unifies theories on bodysize shifts along climatic gradients

Alice Classen, Ingolf Steffan-Dewenter, William J. Kindeketa, Marcell K. PetersImage provided by the authors.

Species traits, like the size and shape of organisms, change along broad-scale climatic gradients. Probably the most famous biogeographical pattern in this context is Bergmann’s rule, which says that species tend to get larger in cooler environments. This has been explained by the fact that species with larger body sizes are energetically favoured because they lose less heat, in relative terms, due to a reduced surface-to-volume ratio. An alternative hypothesis is that energy availability effectively limits the maximum size of organisms. Absolute energy requirements of larger organisms are higher than those of smaller organisms, i.e. they need more energy and space to maintain critical population sizes and are predicted to face higher extinction risks in energy-limited environments. Thus, the predictions concerning body size distributions are contradictory.

Tropical mountains provide excellent conditions to study the patterns and drivers of species traits, as here potential drivers like temperature, area and resource availability change rapidly, making ecological studies feasible. In this study we analysed the body size distributions of wild bees on the highest free-standing mountain in the world, Mount Kilimanjaro (Tanzania). As we assumed that different drivers may operate at different levels of biological organization we studied trends in body size at both the community and species level.

We show that Bergmann´s rule and energy-based predictions are both evident in bee communities along the elevational gradient of Mt. Kilimanjaro. While individuals within species became on average larger with increasing elevation, communities in cooler habitats were increasingly dominated by smaller species. Thus, whether evidence for one or the other hypothesis is found depends on the level of biological organization. We conclude that the integration of intraspecific variation into community ecology can unify conflicting theories on body size shifts along temperature gradients.

Image caption: Image provided by the authors.
Read the article in full here.

Ecosystem ecology

Does differential processing of coral and algal exudates by reef sponges influence dissolved organic matter cycling via the “sponge loop”?

Laura Rix, Dick van Oevelen, Ulrick Struck, Fuad Al-Horani, Christian Wild and Malik NaumannImage provided by authors.

The efficient recycling of nutrients on coral reefs contributes to the characteristic high productivity of these diverse underwater ecosystems. The main primary producers on coral reefs, corals and algae, release large quantities of their excess products from photosynthesis as energy-rich dissolved organic matter (DOM). This DOM represents the largest source of organic matter produced on coral reefs, but most reef organisms that rely on organic matter as a source of energy cannot directly utilize DOM as a food source. Sponges are not only able to consume DOM, but they also transform and release a fraction of the DOM they assimilate as particulate detritus, which can then be used as a food source by many other reef organisms. This sponge-mediated DOM recycling pathway has been termed the “sponge loop” and plays a key role in transferring the energy and nutrients in DOM to higher trophic levels on coral reefs. Interestingly, the DOM released by corals and algae differs in composition and nutritional quality, but the influence of these different DOM sources on recycling by sponges has not been investigated.

We used incubation experiments to compare the processing of coral- and algal-derived DOM by three coral reef sponge species from the Red Sea: Chondrilla sacciformis, Hemimycale arabica, and Mycale fistulifera. We found that the sponges took up and assimilated both coral- and algal-derived DOM into their tissue biomass, but that uptake rates were significantly higher for algal-derived DOM. A substantial fraction (15–49%) of the coral- and algal-derived DOM assimilated by the sponges was subsequently converted into and released as particulate detritus. However, algal-derived DOM was released as detritus at a higher rate. These findings suggest that sponges process and recycle algal-DOM more rapidly than coral-derived DOM. As coral reefs are increasingly threatened by anthropogenic impacts, many corals reefs are undergoing community shifts from coral to algal dominance. By demonstrating that the DOM produced by algae enhances DOM recycling via the sponge loop, our findings have potential consequences for both nutrient cycling and the transfer of energy through food webs on coral reefs.

Image caption: Image provided by authors.
Read the article in full here.


Moose in disturbed forests: impacts on plant regeneration, litter decomposition and soil composition

Nichola Ellis and Shawn LerouxImage provided by authors.

Herbivores, such as moose, can play an important role in ecosystems. By selectively feeding on certain plant species, herbivores can reduce the growth of their preferred plants and promote growth in those plant species they avoid. Herbivores usually consume plants that are relatively high in nitrogen and phosphorus and avoid plants that are relatively high in carbon and non-palatable toxins. Most of the plant material not consumed by herbivores dies and becomes litter which then decomposes in the soil. Depending on feeding preferences, herbivores can dramatically change the concentrations of carbon, nitrogen and phosphorus in the soil. This could influence plant growth, and the insects, birds and other animals that depend on plants.

Evidence from studies in boreal forests in North American show that moose, via their feeding activities, can change plant communities, decrease the amount of carbon, nitrogen, and phosphorus in soils and decrease the time it takes for litter to decompose. We tested the influence of moose and abiotic conditions, such as climate, on plant communities and soils in Newfoundland, Canada, a temperate marine island with different climatic and environmental history from that in other studies.

We used 10 large fenced areas to exclude moose and found that after 15-20 years of moose absence, both preferred and non-preferred plants were able to grow taller, and produce more litter compared to areas where moose were feeding. However, concentrations of carbon, nitrogen, and phosphorus in soils and litter decomposition time were not impacted by moose, while soil depth and soil pH were higher and lower respectively. Our results suggest that, in Newfoundland, environmental conditions such as moisture and disturbance history may have a greater impact on soil quality and litter decomposition than moose presence. We show that future studies of herbivore impacts on forests should consider the importance of environmental conditions. In Newfoundland, Parks Canada should continue to monitor moose populations and forests to see if the effect of moose on forest ecosystems changes over time.

Image caption: Image provided by authors.
Read the article in full here.

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