Lay Summaries

The below summaries are provided by our authors to help put their research paper into context for the wider scientific community and the general public. Lay summaries for the current issue 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

 

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.

 

Variability in potential to exploit different soil organic phosphorus compounds among tropical montane tree species.

Brian S. Steidinger, Benjamin L. Turner, Adrianna Corrales, and James W. DallingGrow house at the Fortuna Forest Reserve.

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The mineral nutrients that plants need to grow and reproduce occur in the soil in a variety of chemical forms. This diversity of form makes it possible for plants to specialize in the acquisition of specific forms, which can reduce competition over growth-limiting nutrients and promote species coexistence. A key nutrient is phosphorus (P), which most plants are helped to acquire by a fungal partner, known as a mycorrhiza. Of the two commonest types of mycorrhiza, one actually penetrates plant roots, while the other forms a sheath around the root.

Previous work suggests plants that associate with these two different functional groups of mycorrhizas differ in their ability to acquire P from organic vs. inorganic sources. We tested this hypothesis at the Fortuna Forest Reserve, a tropical montane forest along Panama’s Central Cordillera, where representative species from both mycorrhizal groups and non-mycorrhizal tree species coexist. First, we collected seedlings of tree species with different mycorrhizal associations from the field, sampled their root systems, and measured the activity of enzymes that allow plants to exploit organic P. Next, we took the same tree species, exposed them to P exclusively in one of four different chemical forms (three organic + one inorganic), and gauged their performance.

Our results confirm that specialized plants that lack mycorrhizal fungi are better able to exploit a specific form of organic P that is unavailable to the mycorrhizal plant species. This difference appears to be related to a markedly higher activity of enzymes that attack organic P. In contrast, we found no evidence that plants associating with different types of mycorrhiza differ in their ability to exploit organic and inorganic forms of P. Overall, our results support the potential for P partitioning to occur in a tropical montane forest, but suggest that it occurs more coarsely among functional groups than previously imagined.

Image caption: Grow house at the Fortuna Forest Reserve.
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.

 

Bolder lizards discard their tails to compensate for risky behavior when food is abundant.

Chi-Yun Kuo, Duncan J. Irschick and Simon P. LailvauxA male brown anole lizard displaying its colorful dewlap. Photograph by Duncan J. Irschick.

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Traits that confer benefits often have costs. A fascinating phenomenon in evolutionary ecology is that individuals can offset the costs of a beneficial trait with the function of another trait (trait compensation). The most common examples of trait compensation are those between behavioral and morphological defense mechanisms, in which individuals that are morphologically more vulnerable tend to show a higher degree of predator avoidance, and vice versa. Despite numerous reports of compensation between defensive traits, two fundamental questions have still not been fully addressed. First, whether trait compensation exists among similarly-aged individuals; and second, whether and how the relationship between compensatory traits would be influenced by the amount of food resource in the environment. Using juvenile brown anole lizards, we examined the relationship between boldness, or a willingness to take risks, and the propensity for employing tail autotomy, a costly defense trait in which a lizard voluntarily discards its tail (which gradually regrows over time), under low and high food availability. We expected bolder lizards to compensate for their higher risk-taking tendency by discarding their tails more readily. We also expected the relationship between the two traits to differ under different food availability, although the exact effect might be complex and difficult to predict a priori. Although lizards raised under low and high food availability on average did not differ in boldness or the propensity for tail autotomy, bolder lizards overall did discard their tails more readily. However, this compensatory effect was present only among individuals raised with abundant food, which suggested that trait compensation was a viable strategy only when lizards can obtain enough food to quickly regrow the lost tails. Our results showed trait compensation existed among similarly-aged individuals and served as a basis for compensatory effects observed at the population, species or higher levels. In addition, we demonstrated that food availability can influence the dynamics between compensatory traits without significantly changing the mean values of the traits per se.

Image caption: A male brown anole lizard displaying its colorful dewlap. Photograph by Duncan J. Irschick.
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.

 

Changes in resource availability have profound consequences for the microbial communities of tropical forest soils.

Nicolas Fanin, Stephan Hättenschwiler, Heidy Schimann & Nathalie Fromin Fungi are main actors of leaf litter decomposition in the tropical forest.

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Tropical forest ecosystems play a key role in the global carbon (C) cycle. In these forests that grow on highly weathered and nutrient-impoverished soils, a mechanistic understanding of how resource availability controls soil C dynamics is urgently needed for accurate predictions of global change effects on the C cycle.

Because soil microorganisms (i.e. bacteria and fungi) have different nutrient requirements, we expected the soil microbial community and the processes it drives to strongly respond to fertilization with different major nutrient elements. We report the results of the first combined fertilization experiment with cellulose (C), urea (nitrogen) and phosphate (phosphorus) in a nutrient-poor tropical rainforest of French Guiana.

After two years of fertilization, we showed that changes in resource availability had profound consequences for soil microorganisms, with clear shifts in the structure and function of the soil microbial community and its ability to process various C substrates. In particular, phosphorus addition enhanced both bacterial and fungal biomasses and overall microbial activity, as well as the ability of the soil microbial community to use a wide range of C substrates. However, the strongest effects of phosphorus fertilization were observed with the simultaneous addition of nitrogen and or C, showing limitation of soil microorganisms by multiple, interacting nutrient elements.

The reported multiple element control of soil microbial biomass, community structure and activity may contribute to a better understanding of spatial and temporal heterogeneity in microbial community structure, their associated functions and the dynamics of C and nutrients in tropical ecosystems.

Image caption: Fungi are main actors of leaf litter decomposition in the tropical forest.
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.

 

Oxidative stress in breeding northern elephant seals.

Jeffrey Sharick, Jose Vazquez-Medina, Rudy Ortiz and Daniel Crocker Photo provided by authors.

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Life history theory suggests that the timing and amount of effort devoted to reproduction over an animal’s lifespan is shaped by natural selection to maximize lifetime reproduction. Central to this theory is the assumption that current reproduction reduces the ability of an organism to reproduce in the future, including negative impacts on survival. This cost may involve allocation of resources to reproduction that reduce energy available for maintenance and health. In some species, called ‘capital breeders’ these trade-offs are distinct as all of the energy used for breeding comes from body reserves stored prior to reproducing. Metabolism produces a variety of reactive oxygen species that can cause damage to biomolecules, and this ‘oxidative stress’ has been theorized to be a potential source of the survival costs associated with reproduction.. Since both high rates of metabolism and fasting are associated with oxidative stress, capital breeders might be especially subject to these costs.

We examined the potential for oxidative stress in breeding northern elephant seals. Since elephant seals forage in the ocean and breed on land, they are capital breeders. Males fast from food for over 100 days while maintaining high rates of metabolism for fighting and mating. Females fast for a month while making one of the most nutrient rich milks found in nature. We compared markers for oxidative stress in males and females at the beginning and end of breeding. We measured a pro-oxidant enzyme that makes reactive oxygen species, three important anti-oxidant enzymes, markers for oxidative damage to fats, protein and DNA, and a marker for inflammation in blood samples. We found that the pro-oxidant enzyme increased across breeding and the seals responded by increasing the levels of anti-oxidant enzymes. Despite this protective response, males showed evidence of oxidative damage to fats and DNA and showed increased levels of inflammation. Females showed evidence of oxidative damage to proteins. Our results provide evidence for oxidative stress as a cost of breeding in polygynous male elephant seals and weaker evidence in females. These data support the idea that oxidative stress may underlie survival impacts of reproduction in some species.

Image caption: 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.

 

Swimming loss and recovery in the Atlantic silverside.

Kestrel Perez & Stephan MunchAdult Atlantic silversides collected in little neck bay, Long Island, NY USA. Photo credited to Kestrel O. Perez..

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For many animal species, large body size leads to higher survival and reproductive success. Because fast growth rates enable an individual to obtain a large body size sooner, it stands to reason that fast growth should be similarly beneficial. Why then, do growth rates commonly still vary in many species? In fact, most species do not grow as fast as possible, suggesting that there must be some down-sides to rapid growth. Across a wide range of animal species, there have been many documented cases of the negative effects of fast growth. One such example is the Atlantic silverside, a common marine fish, where individuals that grow rapidly have poorer swimming ability compared to slow-growing individuals of the same size. But, how long this effect lasts is currently unknown. In this study, we determined how long it takes for a fish to recover its ability to swim following a period of fast growth. We manipulated growth rate in Atlantic silversides by providing variable amounts of food, either unlimited food for the fast growth treatment or limited food for the slow growth treatment. After two weeks of these feed rations we then fed both treatments limited rations to maintain slow growth rates. We monitored swimming ability over this period. Full recovery from the effects of earlier fast growth would be indicated if swimming ability of the fish that had previously been growing fast, but were currently growing slowly, improved and became comparable to swimming ability of the fish that had always been growing slowly. Interestingly, we found that fish that had grown rapidly early in life not only had significantly poorer swimming ability, but continued to show the effects of this early period of rapid growth. We found that fish fully recovered normal swimming ability only after 1 month of growing slowly. Most surprisingly, swimming ability actually decreased before it improved.

Image caption: Adult Atlantic silversides collected in little neck bay, Long Island, NY USA. Photo credited to Kestrel O. Perez..
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.

 

Community phylogenetics and ecosystem functioning

Clarifying the discussion of how environmental variation shapes community diversity.

Nathan J. B. Kraft, Peter B. Adler, Oscar Godoy, Emily James, Steve Fuller & Jonathan M. LevineIn the Central Valley of California, USA, small depressions in the ground can fill with rainwater in the winter, creating a vernal pool habitat. The dominant plant species (shown here in bloom) that are found in these pools can tolerate immersion in the rainwaters, while the flooded conditions exclude many of the surrounding grassland species. This process of environmental filtering, seen here at a small scale, shapes patterns of biodiversity across the planet. Credit: Nathan Kraft.

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Variation in environmental factors such as temperature, rainfall and soil chemistry have profound effects on the distribution of biodiversity across the planet. Community ecologists often use the concept of "environmental filtering" to describe situations when a species is unable to survive at a site because of the environmental conditions. However, the evidence that ecologists have used to test for environmental filtering in the past is often indirect, as it is not always sufficient to rule out other potential causes, such as competition with other species. This uncertainty is particularly problematic if we try to use results from these studies to make predictions about how global change will impact species and communities.

In this study we describe a conceptual framework to help distinguish environmental filtering from other sources of variation in community structure. Strong evidence for environmental filtering comes from showing that species have the potential to arrive at a site (as a dispersed seed or as a migrant from a nearby area, for example) but are unable to survive in the environmental conditions found there. We reviewed the ecological literature to assess how environmental filtering is typically assessed, and despite the widespread use of the concept, only 15% of published studies included this direct evidence. Most studies instead rely on patterns such as species changes in abundance or changes in physiological characteristics across an environmental gradient, patterns that can be driven by other factors.

We discuss a number of ways in which both experimental and observational studies can be improved to give a more precise accounting of the role of abiotic variation in shaping community structure. By addressing these issues, ecologists can come to a clearer understanding of the multitude of ways in which environmental variation shapes patterns of diversity across communities.

Image caption: In the Central Valley of California, USA, small depressions in the ground can fill with rainwater in the winter, creating a vernal pool habitat. The dominant plant species (shown here in bloom) that are found in these pools can tolerate immersion in the rainwaters, while the flooded conditions exclude many of the surrounding grassland species. This process of environmental filtering, seen here at a small scale, shapes patterns of biodiversity across the planet. Photo credited to Nathan Kraft.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plant uptake elements as influenced by phylogeny, soil and climate.

Zhuan Hao, Yuanwen Kuang & Ming KangPrimulina bullata growing calcareous soils (Photo credit: Ming Kang).

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Plants require a large number of chemical elements to sustain their life. Understanding factors that influence elemental composition of plants is important because it provides insight into a wide range of ecological and environmental processes. Numerous experimental studies have previously documented the influence of soil and climate on elemental composition of plants, but phylogeny is still rarely considered as a factor in determining plant elemental contents (i.e. whether closely related species have similar elemental composition, even in different environments). In this study, we measured leaf concentrations of seven elements and evaluated soil properties for 177 species of the African violet subfamily Didymocarpoideae from subtropical China, a global biodiversity hotspot. We partitioned the variation in leaf element contents into the effects of soil, climate and phylogeny. Then we tested whether closely related species tend to have similar ecological characteristics (i.e. phylogenetic signal) at two different phylogenetic scales (subfamily vs genus). We also used phylogenetic comparative methods to assess the impacts of soil and climatic conditions on leaf element concentrations.

We detected a strong phylogenetic signal in leaf elements as well as for soil and climate variables at the subfamily level, whereas the large genus Primulina exhibits no significant phylogenetic signal in leaf elements or in most soil variables. We found an influence of both soil and climatic conditions on leaf element concentrations. However, the patterns of the relationships between leaf elements and soil and climate variables vary at the subfamily and genus levels. Phylogeny has a stronger effect than soil and climatic factors on leaf element contents at the subfamily level, while leaf elements within the genus Primulina are mostly influenced by environmental conditions. We conclude that the influences of taxonomy, soil and climate on leaf element concentrations are dependent on the phylogenetic scale of analysis, highlighting the need to integrate phylogenetic scales to explore the influence of soil and climatic conditions on leaf element concentrations.

Image caption: Primulina bullata growing calcareous soils (Photo credit: Ming Kang).
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.

 

Hard work, dominance and health in a Kalahari bird.

Dominic L. Cram, Jonathan D. Blount & Andrew J. YoungFemale white-browed sparrow weaver in an Acacia tree. Credit Dominic Cram.

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When groups of animals live together (including humans), they often divide workloads, and some individuals work harder than others. Are the hardest-working individuals the healthiest, and does this allow them to work harder than everyone else? Does their work-rate impact their health, leaving the hard-workers in poor condition?

We investigated these questions in groups of white-browed sparrow weavers, in the Kalahari Desert. Although they share workloads as ‘cooperative breeders,’ within each group the dominant male and female work much harder than the subordinates. Dominants are the only birds that breed, with dominant males singing to attract their mate and dominant females producing all eggs and providing most of the care for nestlings. Both dominants also work hardest to defend the group’s territory. How do the unequal workloads of dominants and subordinates relate to their health?

We focussed on one aspect of the birds’ health: oxidative status. Previous studies have shown that hard work can increase the generation of harmful free radicals. Antioxidant defences help animals protect themselves, but if this protection is overwhelmed, oxidative stress can result. Oxidative stress is thought to be involved in many diseases and ageing.

First, we blood-sampled 93 birds before the breeding season began, to look at whether dominants (the hard-workers) had better oxidative states than subordinates, with stronger antioxidant protection and lower oxidative damage. We found that, in fact, there were no differences between dominants and subordinates in oxidative states before breeding.

Next, we sampled the same 93 birds after their long breeding season, to examine whether the dominants’ hard work during the intensive six months of breeding left them exposed to oxidative stress. After the breeding season, we found that dominant females (the hardest workers) were suffering from weakened antioxidant protection, compared to their subordinates.

Our study suggests that differences in oxidative status may not lead to differences in work-rates, but that unequal sharing of workloads in animal societies can leave the hardest-workers with poor antioxidant protection. This could leave those working hardest at higher risk of poor health, and could lead to accelerated ageing.

Image caption: Female white-browed sparrow weaver in an Acacia tree. Credit Dominic Cram.
This article can be found here.

 

Is the energy expenditure of free-living animals linked to their metabolic costs at rest?

Jorg Welcker, John R. Speakman, Kyle H. Elliott, Scott A. Hatch and Alexander S. KitayskyKittiwakes breeding at the study site on Middleton Island, Alaska, USA. Photo  by Jorg Welcker.

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Reproduction is energetically costly and the overall rate at which animals expend energy is usually highest when they rear their young. The overall rate of energy expenditure integrates the energy an animal spends to raise its offspring and to keep its own body up and running. The resting metabolic rate, on the other hand, measures the minimal energetic cost to an animal at rest to maintain its body tissues.

A widespread assumption is that an increase in parental energy expenditure requires a concurrent increase of the resting metabolic rate as higher energy intake and expenditure would need to be facilitated by larger or metabolically more active internal organs such as the heart, liver or alimentary tract. Larger or costlier metabolic machinery would, in turn, result in higher resting energetic costs. However, if changes in resting and overall energy expenditures were not inherently linked, it could be beneficial for animals to reduce their resting energetic costs as they could thus increase the amount of energy spent on raising young.

We examined whether this might be the case in free-living kittiwakes. We manipulated the energy demands of parents by increasing the number of chicks in their nests or by removing entire broods. We also manipulated energy supplies by providing some nests with supplemental food.

We found that overall and resting metabolic rates were not inherently linked: birds that raised chicks had higher overall energy expenditure yet lower resting metabolic costs compared to birds that had their broods removed. Overall energy expenditure was constrained as neither parents of enlarged broods nor those provided with unlimited food spent more energy than controls. Thus, our results suggest that reducing resting energetic costs is a strategy to increase the amount of energy allocated to raising young when overall energy expenditure is constrained. The increase in energy allocated to chick rearing caused higher levels of stress incurred by parents, suggesting that such a strategy might be costly to the parental birds.

Image caption: Kittiwakes breeding at the study site on Middleton Island, Alaska, USA. Photo by Jorg Welcker.
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.

 

Less is more: choosy wasps used in biological control show why a diverse diet is not always an asset.

Silvia Rossinelli and Sven Bacher Parasitic wasp searching for its leafminer host.

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The question of why species should specialize, i.e. use only a fraction of all resources available to them, has puzzled scientists and non-scientists alike. The proverbial saying "the Jack of all trades is master of none" provides an intuitive explanation. It implies that there should be a trade-off between the ability to use many different resources and the efficiency of using each single one. Thus, specialists should gain advantages on their resource compared to generalists. However, empirical tests so far have had problems showing such trade-offs and their importance for the evolution of specialization is still debated.

Parasitic wasps are one of the largest insect groups with maybe more than 1 million species. They parasitize other insect species by laying their eggs upon or inside the host’s body, where hatching larvae develop and eventually kill the host. For about 100 years, parasitic wasps have been widely used for the biological control of insect pests worldwide. Within this insect group all degrees of diet breadth are found, however, narrow host ranges prevail.

We analysed the history of parasitic wasps that were released to control pest insects and found that specialised wasps, i.e. those that can only parasitize a few pest species, establish better than generalist species with a wide host range. Thus, this is the most comprehensive test for the hypothesis that specialists are generally better able to use their hosts than generalists. The results provide the first robust support for the general importance of trade-offs in the evolution of specialization in the mega-diverse group of parasitic wasps. However, specialization is not always more advantageous; in environments where the preferred host is not always available, generalists will profit from being able to utilise a variety of different hosts.

Image caption: Parasitic wasp searching for its leafminer host.
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.

 

Food jumpstarts feather moult.

Raymond M. Danner, Russell S. Greenberg, Julie E. Danner and Jeffrey R. WaltersA swamp sparrow moulting throat, face, and crown feathers in eastern North Carolina.  Photo by Jeff Lewis, used with permission.

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Moulting (periodic loss of old feathers and growth of new ones) is critical for many bird species, but it costs both time and energy. Moulting may interfere with other important activities, such as breeding, migration, and maintaining body heat. Therefore, the timing of moult is essential for ensuring a successful year. In birds, the prebreeding moult is especially important because it may delay breeding. The prebreeding moult is also when males of many species acquire colourful plumage that is important for attracting mates and competing with other males.

The end of the winter is a lean time for many birds because food resources have been depleted since the previous fall. We hypothesized that the scarcity of food in late winter inhibits the initiation of prebreeding moult. We experimentally tested, for the first time, if food abundance influences the timing of moult in the wild. We conducted a controlled food supplementation experiment on free-living swamp sparrows (Melospiza georgiana) preceding and during the time of natural prebreeding moult (January–March 2009, 2010).

Supplemented birds began moulting the body, face, and crown earlier than control birds (11, 14, and 8 days earlier, respectively) indicating that food abundance limits the initiation of moult. Along with interannual variation in moult timing, these results indicate that day length is not the sole cue for moult initiation. Both control and supplemented birds moulted in sequence, starting with the body, followed by the crown 9 days later, and the face 11 days later. The presence of a sequence further suggests energetic limitation of moult or possibly a strategy to moult specific regions first to ensure completion at an optimal time.

This study provides novel experimental evidence that food abundance can limit moult timing in the wild. Food limitation of moult timing could affect the timing of breeding or feather quality, and thus cascade through other life history stages in the annual cycle and ultimately affect reproductive success. These results indicate that food availability is a cue for moult initiation, possibly acting secondarily to photostimulation.

Image caption: A swamp sparrow moulting throat, face, and crown feathers in eastern North Carolina. Photo by Jeff Lewis, used with permission.
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.

 

Stress hormones regulate how the past can affect the future in wild banded mongooses.

Jennifer L. Sanderson, Andrew J. Young, Sarah J. Hodge, Solomon Kyabulima, Susan L. Walker & Michael A. Cant A banded mongoose (Mungos mungo) pup on the Mweya Peninsular, Western Uganda. Photo credit: Jennifer Sanderson.

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Virtually every decision that you make will affect your later life. For example, a decision to work hard can leave you tired and less likely to work hard the following day. In ecology this is called a ‘carry-over effect’. Such carry-over effects are widespread in animal populations and may explain why individuals with high parental investment in one breeding attempt often invest relatively little in a second breeding attempt.

Evidence suggests that carry-over effects arise when the energetic losses from previous parental investment persist into the next breeding attempt. However, little is known about the physiological mechanisms that regulate these effects. Here, we test the hypothesis that carry-over effects arise because working hard to raise offspring causes increased concentrations of stress hormones (glucocorticoids; GCs), which inhibit future parental investment. Our field study of wild banded mongooses provided strong support for this hypothesis, and suggests that factors known to influence an individual’s stress physiology can have lifelong impacts on reproductive behaviour and fitness.

The banded mongoose is a close relative of the meerkat and is found living in stable social groups across Central and Eastern Africa. Banded mongooses breed cooperatively; all individuals assist in offspring care even if they do not breed themselves. We collected faecal samples and behavioural observations from banded mongooses living on the Mweya Peninsular in Western Uganda to investigate if GCs mediate a carry-over effect whereby individuals that invest heavily in cooperative offspring care in one breeding attempt invest little in the next.

Banded mongooses that entered a breeding attempt with low GCs fed pups more often than individuals with high GCs, suggesting that elevated GCs inhibit offspring care. High investment in offspring care led to an increase in GCs during the breeding attempt, and this elevation persisted after the care period. Furthermore, supplementary feeding of carers led to a decrease in GCs, confirming that this GC increase is due to energetic losses. Our results provide new insight into the physiological regulatory mechanism behind carry-over effects and a better understanding of how stress associated with the past can affect behaviours in the present.

Image caption: A banded mongoose (Mungos mungo) pup on the Mweya Peninsular, Western Uganda. Photo credit: Jennifer Sanderson.
This article can be found here.

 

Nutritional geometry of the giant panda.

Yonggang Nie, Zejun Zhang, David Raubenheimer, James J. Elser, Wei Wei and Fuwen WeiPhotograph caption: Giant panda feeding on wood bamboo shoot. Photo credited to Fuwen Wei.

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Many studies have shown that herbivores face nutritional challenges, including plant-produced toxins and nutritionally imbalanced foods. These challenges, which can have significant influences on critical aspects of animals’ life cycles including longevity and reproduction, may become more acute under ongoing climate change. This is especially true for species that live in seasonal environments. In response to such challenges, animals have evolved behavioral, developmental, and physiological adaptations to meet their demands for various nutrients and maintain performance.

The giant panda (Ailuropoda melanoleuca) is a unique species in the order Carnivora that evolved to specialize on various species of bamboo, which are generally thought to be of poor nutritional quality due to low protein and high fiber and lignin contents. The giant panda may thus face particularly acute nutritional challenges. Previous studies have highlighted many ecological and life history characteristics that might be associated with the ability of panda populations to survive as bamboo specialists. For example, pandas have a seasonal reproductive pattern with mating in spring and birth in fall which is believed to be an ecological adaptation to different seasonal nutritional environments.

We combined behavioral observations of food selection with analysis of the calcium, phosphorus, and nitrogen (as a proxy for protein) composition of foods and matched feces, to determine how the panda's distinctive seasonal habitat choice and food selection relate to its nutritional balance. Our results showed that pandas displayed marked foraging changes, with four primary foraging periods corresponding to the annual life cycles of the two bamboo species that make up most of its diet. These foraging changes are also coupled to its seasonal migration between low and high elevations. Analysis suggests that the pattern of migration coupled with seasonal diet switches were necessary to obtain a diet balanced in calcium, phosphorus and protein, and likely play an important role in the life cycle and reproduction of giant pandas. These results have potentially important implications for habitat conservation for giant pandas, suggesting that the summer and winter habitats of giant pandas are not nutritionally interchangeable, but provide complementary nutrition required to complete the life cycle.

Image caption: Photograph caption: Giant panda feeding on wood bamboo shoot. Photo credited to Fuwen Wei.
You can find the article here.

 

Ageing gracefully: physiology but not behaviour changes with age in a diving bird.

Kyle H. Elliott, James F. Hare, Maryline Le Vaillant, Anthony J. Gaston, Yan Ropert-Coudert and W. Gary AndersonMurres in flight. Photo provided by authors.

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How can long-lived wild birds both work hard and live long? We examined this question by studying murres (also known as guillemots) aged 3-30 years. Murres have the highest flight costs, for their body size, of any flying animal. They dive exceptionally deep for their body size (over 150 m for five minutes). Yet they also have exceptionally long lives for their body size; they live decades longer than rabbits, which weigh roughly the same. To examine how metabolism changes with age in wild murres, and how that affects dive performance, we measured oxygen consumption, oxygen stores and dive behaviour. Both oxygen stores and oxygen consumption rate declined with age, which we suggest reduces the effect of high metabolism on ageing. In contrast, there was no change in dive performance with age; old murres dove as deep, for as long and spent as much time recovering at the surface as young murres. Thus, multiple physiological systems changed in tandem with advancing age in murres, and offset each other such that there was no detectable decline in behavioural performance. Murres were able to maintain their ‘healthspan’ into old age.

Image caption: Murres in flight. 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.

 

Pesticide chronically affects bee foraging.

Richard J. Gill & Nigel E. RaineBumblebee foraging on clover. Photo and permission provided by Steve Gill.

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Bees provide an essential environmental service by pollinating many wild flowers and key agricultural crops. The importance of these critical pollinators, both economically and for continued food security, make it particularly concerning that bees are suffering global declines. Pesticide exposure has been suggested as one of many possible factors driving bee declines. Although the levels of pesticide to which bees are exposed in the field are typically not lethal to bees, they may still produce sublethal effects, such as changes in behaviour leading to problems with colony function.

In this study we investigated how two commonly used pesticides affect the foraging behaviour of individual workers of bumblebees at approximately field relevant exposure levels. We examined the responses of bees and their colonies following short-term (acute) exposure, and (chronic) exposure over an extended period of time. Bumblebees are social insects, meaning the colony consists of a queen that lays almost all the eggs, accompanied by numerous workers that help to rear the brood, protect the colony and importantly go out to forage by collecting pollen and nectar from flowers. Therefore, understanding whether pesticides impair foraging behaviour is important because this can have detrimental consequences for colony growth and reproductive success. We attached Radio Frequency Identification Tags to automatically record all foraging trips made by each bee. Using this technology we recorded the natural activity patterns of 259 foraging workers from 40 bumblebee colonies over four weeks.

This is the first study to provide data on the impacts of pesticide exposure on the day-to-day dynamics of bee foraging behaviour in the field over a prolonged period of time. Our results showed that a neonicotinoid pesticide (imidacloprid) had both acute and chronic effects on overall foraging activity. Colonies exposed to the neonicotinoid recruited foragers at a higher rate over the four week period than control colonies, an effect that appeared to be a response to impaired individual foraging efficiency. While individual foragers from control colonies improved their pollen foraging performance as they gained experience, the pollen foraging performance of bees exposed to the neonicotinoid became worse. At the colony level, we observed that the proportion of neonicotinoid exposed foragers that successfully collected pollen decreased as the experiment progressed. There was also evidence to suggest forager preferences for particular flower types were affected by neonicotinoid exposure. Our findings highlight the importance of considering prolonged exposure when assessing the risk that pesticides pose to bees.

Image caption: Bumblebee foraging on clover. Photo and permission provided by Steve Gill.
This paper can be found free online here.

 

Maternal effects influence phenotypes and survival during early life stages in an aquatic turtle.

Timothy S. Mitchell, Jessica A. Maciel and Fredric J. JanzenA hatchling painted turtle emerges from the nest after winter.

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Many egg-laying animals do not care for their young, but this does not mean that good mothering is not important for offspring. For such animals, there are two maternal effects that are particularly important: nest-site choice and egg size.

We explored the importance of such maternal effects in the painted turtle (Chrysemys picta). By selecting particular microhabitats at the time of nesting, the mother turtle can partially influence the abiotic conditions her eggs will experience during incubation and the hatchlings will experience as they overwinter within the natal nest. This abiotic environment is very important for two reasons: it can shape phenotypes of developing offspring via phenotypic plasticity, and it can act as a selective force. In this field experiment, we compared offspring incubating and hibernating in maternally-selected nests to those in randomly-selected nests. Our results show that mothers selected nests that were relatively open (unshaded), and this resulted in maternal nests being significantly warmer than random nests during incubation. Hatchlings from these maternal nests were longer and developed faster than their counterparts in random nests. However, the ability to modify thermal environments of the nest faded during the overwinter stage. There was a weak correlation between vegetation cover and nest temperature, and maternal and random nests experienced similar thermal environments.

We also tracked individual eggs and hatchlings, and showed that larger eggs produce larger hatchlings. These larger hatchlings had a higher probability of surviving winter, where experiencing lethally cold temperatures was a substantial source of mortality. This novel result provides further support for the “bigger-is-better” hypothesis in early life stages of freshwater turtles.

In the turtle world, three clichés ring true: mother knows best, size matters and location is everything (or at least, it is very important).

Image caption: A hatchling painted turtle emerges from the nest after winter.
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.

 

Do eggshells act like sunscreen?

Golo Maurer, Ivan Mikšík, Steven J Portugal, Mark E Hauber, Douglas Russell, Phillip CasseySong thrush eggs. Photo provided by authors..

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The eggs of birds have an amazing array of adaptations to ensure the safety of the embryo developing inside. Such adaptations can include camouflage of the shell to help protect against predation, special pores that allow the correct amount of air into the egg and infection-fighting pigments to help the embryo fight disease. One important aspect the shell of the egg must control is the amount of light that penetrates through to reach the embryo. Too much light penetrating the eggshell will result in lethal levels of radiation from the UV light, but too little light can cause embryo deformities and increase the likelihood of disease. Therefore, the eggshell has to ensure that just the right amount of light is allowed through the shell. Birds nest in a wide range of environments and habitats, including extreme temperatures, altitudes, in burrows, on cliffs; how does the egg of each species in differing environments make sure the right amount of light reaches the embryo? We examined how the eggshells of British breeding birds have adapted to different environments, and how different shells control the amount of light that reaches the embryo. We found that the eggs of species that nest in burrows, holes and other closed environments let more total light pass through the eggshell, compared with species that nest in the open. Specifically, we show that less light passes through thicker eggshells with greater total pigment concentrations. The pigment potentially acts like sun-block. It seems, therefore, that greater light transmission through the shell is required to assist embryonic development under low-light exposure. To make sure enough light gets through to the embryo in these dimly-lit conditions, eggs of birds that nest in burrows and holes are white, allowing more light in as there is less pigment to block the sun. For birds who have a long incubation period (exposing their eggs to the sun for longer), their eggs are often dark with pigment, letting significantly less of the potentially harmful, ultraviolet (UV) light pass through the eggshell.

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

 

Daily energy expenditure during lactation is strongly selected in a free-living mammal.

Quinn E. Fletcher, John R. Speakman, Stan Boutin, Jeffrey E. Lane, Andrew G. McAdam, Jamieson C. Gorrell, David W. Coltman and Murray M. Humphries Female red squirrel with one of her pups outside of her grass nest. (Photo credit: Ryan W. Taylor).

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Energy is a currency of life because all animals must expend it to survive and reproduce. Despite the importance of energy as a currency, we know very little about the benefits and costs associated with the amount of energy that animals expend. Past research on mammals has demonstrated that lactation is an energetically costly time of the year because females must expend energy to forage for food, and synthesize milk to raise multiple offspring. We found that the female North American red squirrels that expended the most energy during lactation had the most offspring survive to the following year (i.e. they have greater reproductive fitness). At first glance, it makes intuitive sense that there would be reproductive fitness benefits associated with expending large amounts of energy during lactation. However, our results are interesting because they raise a series of mysteries. The first set of mysteries relates to the mechanism by which elevated energy expenditure during lactation is associated with greater reproductive fitness. The most obvious mechanism is that females that raise larger litter sizes or healthier offspring (i.e. faster growing) have more offspring survive to the following year, but also need to expend more energy to do so. However, this mechanism appears not to be true because there is no relationship between a female’s energy expenditure during lactation and either its litter size or the growth rate of its offspring. Moreover, in order for juveniles to survive until the following year, they must first obtain a territory, then hoard enough cones to survive the winter, and then evade a suite predators. Our results are definitely a mystery because they suggest that if pups are raised by females that expend elevated levels of energy, that this somehow helps them to survive these ecological challenges. The second mystery relates to our finding that females that expended the most energy during lactation experienced no negative consequences. Specifically, we found that females with high levels of energy expenditure during lactation had neither reduced survival to the following year, nor a decreased ability to invest in reproduction the following year. These results are interesting because if there are benefits associated with expending energy during lactation, but no costs, why do not all females expend energy at a high rate?

Image caption: Female red squirrel with one of her pups outside of her grass nest. (Photo credit: Ryan W. Taylor).
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.

 

Subdigital adhesive pad morphology varies in relation to structural habitat use in the Namib Day Gecko.

Clint E. Collins, Anthony P. Russell, and Timothy E. Higham Rhoptropus afer pauses before ascending a granite outcrop.

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Locomotion is a quintessential aspect of animal life. Effective locomotor performance is crucial for many important tasks such as prey capture, mating, and predator evasion. Gecko locomotion is fascinating because of the specialized adhesive capability that allows them to live on vertical and inverted surfaces. Adhesion is finely controlled by the subdigital toe pad and the millions of microscopic, hair-like structures known as setae that are located on the bottom of each toe pad. However, this specialized behaviour and the adhesive system comes at a cost – running away from predators on level surfaces may be affected owing to the complexity and timing of adhering and detaching to surfaces during locomotion. Quantifying the interplay between escape behaviour and locomotor morphology across habitats that vary in structural composition could reveal how selection acts on locomotion at local levels.

Our study found that in habitats where escape behaviour relies on flatter surfaces, a species of gecko, Rhoptropus afer, the Namib Day Gecko, has exhibited a greatly reduced adhesive morphological system. We investigated the impact of habitat variation and escape behaviour on morphology, including the adhesive system, of Rhoptropus afer, a diurnal and cursorial (adapted to running) gecko from Namibia. Substrate incline and topographical variation are likely important for this pad-bearing gecko due to the trade-off between adhering and sprinting (i.e. using adhesion results in decreased sprint speed) that is triggered by certain inclines. We corroborate the hypothesis that the adhesive system exhibits the greatest degree of reduction in populations that utilize the flattest terrain during an escape. Our findings suggest that the adhesive apparatus is detrimental to rapid locomotion on relatively horizontal surfaces, and may thus be counterproductive to the evasion of predators in such situations.

Image caption: Rhoptropus afer pauses before ascending a granite outcrop.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

How to best assess the cold tolerance of Drosophila.

Jonas Lembcke Andersen, Tommaso Manenti, Jesper Givskov Sørensen, Heath Andrew MacMillan, Volker Loeschcke and Johannes OvergaardImage supplied by authors.

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Insects represent around three quarters of the world’s named species and they often play an important role in human society as pollinators, agricultural pests or carriers of disease. Insects’ distribution across the globe is partially limited by their ability to survive cold. In order to predict changes in the patterns of insect distribution across the world we need to understand how cold affects insects and how some insects survive for hours below 0°C while others die after only short exposures to low temperatures.

Many of the studies done on insect cold tolerance (temperatures that limits insects’ ability to survive, reproduce, or migrate) have been performed with fruit flies (Drosophila) utilizing several different methods to assess cold tolerance. In this study we evaluated the accuracy of cold tolerance estimates obtained using five commonly used methods. We assessed the cold tolerance of 14 Drosophila species using each of the 5 methods. An average natural latitudinal distribution and an expected minimum temperature exposure was determined for each of the species using databases with thousands of observations. These parameters were then correlated to each of the five cold tolerance measurements to investigate which method was best correlated to the actual distribution and minimum temperature exposures of the 14 species in the wild.

We found that the temperature where the flies lost their ability to move (chill coma onset), when ramping down the temperature, had a strong correlation to the environmental variables. So did measurements of survival after 2 hours of low temperature exposure (lethal temperature) as well as survival time at milder low temperatures (lethal time). However, the time it took the flies to recover from cold shock (chill coma recovery time) had a weaker correlation to the environmental variables and supercooling point, the temperature where the flies freezes over, had the weakest correlation to distribution and estimated temperature exposure.

Considering the amount of time involved and the difficulty of making the different measurements, we found that chill coma onset and lethal temperature are superior measurements when estimating cold tolerance in Drosophila.

Image caption: Image supplied 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.

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