Who’s the big bad wolf afraid of? Investigating how humans affect the predatory behavior of wolves

This blog post is provided by Kristin Barker and tells the #StoryBehindthePaper for the paper “Large carnivores avoid humans while prioritizing prey acquisition in anthropogenic areas“, which was recently published in Journal of Animal Ecology. In the study, they investigate the impact of human activity on the behaviour of grey wolves, finding a nuanced response to different human influences depending on the context.

Right now, populations of large carnivores like grizzly bears and grey wolves are recovering across the globe. There’s a common story in ecology that these predators deliberately avoid humans, and many of our key ecological theories hinge on this story. For example, we attribute the increasing use of human areas by ungulates (hooved mammals) to the reduced predation risk afforded by large carnivores’ avoidance of humans. But livestock producers and others who live in carnivore recovery areas share stories of large predators killing and eating prey right in front of humans with no apparent avoidance response.

A wolf stands on the National Elk Refuge in Jackson Hole, Wyoming, USA. (Photo credit: Mark Gocke, Wyoming Game and Fish Department)

To reconcile the disparity between our expectation that large carnivores should avoid humans and the reality that sometimes they don’t, we need to understand how these animals perceive and respond to humans. Are large carnivores scared of humans only if we directly threaten them, for instance by hunting? Or are they not scared at all, but rather just generally disturbed by human activity, in which case we would expect a weaker but more generalized avoidance of humans? It’s also possible that carnivores are attracted to human areas where ungulate prey concentrate in predictable places and times, but it’s not clear whether this potential food benefit might outweigh the costs of potentially interacting with humans. Teasing apart carnivore perception of humans could help resolve some of the uncertainty around carnivore responses to humans in different contexts. 

To answer these questions, and to investigate whether human-induced behavioral changes in large carnivores affect the risk of predation for their ungulate prey, we launched a new field campaign in the southeastern Greater Yellowstone Ecosystem, USA. Over the course of three winters we skied, snowshoed, waded, and snowmobiled to more than 1000 potential wolf kill sites. We then contrasted characteristics of the 170 wolf kills we found with those of matched non-kill sites to quantify how predation risk changed as a function of human influences, while controlling for key environmental factors. Specifically, we evaluated the effects of roads, trails, and human-run ungulate feedgrounds, and we also investigated whether wolves responded more strongly to these influences if they had previously been hunted by humans and/or if it was during the day when humans were most active.

Field technician Celeste Governale bootpacks along a ridge to access a wolf kill site in southeastern Jackson Hole. (Photo credit: Kristin Barker)

We found that wolves did change their predatory behavior in response to humans, but they didn’t unequivocally perceive humans as either scary, disturbing, or beneficial. Instead, wolves in our study area actively distinguished between different types of human influences based on the immediate costs and benefits of each. For example, we found opposite responses of wolves to roads and trails. Wolves preferentially made kills far from paved, plowed roads but close to unplowed oversnow trails, despite plowed roads making it much easier to travel through the snowy landscape. However, wolf response to human influences was much weaker – and in some cases nonexistent – in areas where prey availability was particularly low. Furthermore, despite their preference for using unplowed trails to access their prey, wolves avoided killing prey near trails during the day when humans were most likely to be using them. 

Struggling to ski uphill in the Gros Ventre River drainage, field technician Celeste Governale becomes intimately acquainted with the influence of snow depth on animal movement. (Photo credit: Kristin Barker)

This nuanced response of wolves to different human influences helps clear up superficially incongruous results from other studies and personal observations. Based on our finding that wolves actively differentiate between the immediate risks and rewards of multiple simultaneous human influences, it is not surprising that wolves respond very differently to humans in different contexts. Our work suggests that the degree to which wolves alter their predatory behavior hinges on the availability of ungulate prey in conjunction with the intensity or predictability of human use. In particular, in areas where prey are scarce, wolves may be unlikely to prioritize avoiding humans over acquiring prey despite their general avoidance of human activity. In the next phase of our research, we are building on these findings to investigate how the responses of wolves to humans can directly and indirectly affect populations of their native prey.

Field technician Hannah Booth performs a necropsy at a potential wolf kill site along the Snake River. (Photo credit: Becca Lyon)

As populations of large carnivores continue to recover across the globe, they will inevitably continue to expand into human-dominated areas. Wildlife managers, conservationists, policymakers, and local stakeholders all have a vested interest in anticipating and responding to the ecological and socioeconomic effects of carnivore recovery. By unveiling some of the nuance behind wolf response to humans, we hope our work can help inform strategies to mitigate concerns related to human-wildlife conflict, prey population dynamics, and undesirable ungulate distributions in human-dominated areas.

Wolves and elk share the landscape with humans in Jackson Hole, Wyoming (filmed by Mark Gocke of the Wyoming Fish and Game Department)
Read the paper

Read the full paper here: Barker, K J., Cole, E., Courtemanch, A., Dewey, S., Gustine, D., Mills, K., Stephenson, J., Wise, B., & Middleton, A D. (2023). Large carnivores avoid humans while prioritizing prey acquisition in anthropogenic areas. Journal of Animal Ecology, 00, 1– 12. https://doi.org/10.1111/1365-2656.13900

Prophylactic antibiotic use and its consequences for snails’ ability to cope with predators

This blog post is provided by Denis Meuthen and tells the #StoryBehindthePaper for the paper ‘On the use of antibiotics in plasticity research: gastropod shells unveil a tale of caution’, which was recently published in Journal of Animal Ecology. In the study, they look at how antibiotic exposure affects shell-thickness responses in the snail Physella acuta, which is known to develop thicker shells in the presence of predators.  

You might be aware of the antibiotic crisis that plagues our planet. Their prophylactic use, without consideration for aftereffects, is widespread among some animal farmers, veterinarians and even medical doctors. This practice has already led to the emergence of multidrug-resistant bacteria strains that are responsible for the death of many people. However, the consequences of prophylactic antibiotic treatment for animals are much less known.

Animals have evolved an ability that allows them to cope with sudden changes to their environment. When environmental changes happen, they can alter their hormone levels or DNA expression, and this can modify the behaviour, morphology and life-history of animals. This is known as phenotypic plasticity. This ability is crucial also in the face of predators. This is because when prey animals perceive the presence of predators, they can ensure the survival of their genes by escaping, by forming strong defences or by reproducing earlier.

A well-studied and common defence that is caused by the presence of predators are thicker shells in the snail Physella acuta (Figure 1). When these snails smell dead conspecifics, they invest energy into making their shells thicker so that predators cannot crush them anymore. However, studying these snails is not easy as many of them die in the laboratory during the course of an experiment. In a recent study, Thomas DeWitt and Heather Prestridge suggest that prophylactic antibiotic treatment may reduce snail mortality. They also singled out the antibiotic erythromycin to be the most efficient one for this purpose.

Figure 1: Our model organism Physella acuta. Photo by Robert Aguilar, Smithsonian Environmental Research Center, used under CC BY 2.0.

We were now interested in studying how a prophylactic treatment with erythromycin affects the ability of snails to form a thicker shell. For this purpose, we set up four treatments. Exposure of snails to either an antibiotic or a control water treatment was followed up by either exposure to the smell of dead conspecifics (high-risk) or a water control (low-risk). Antibiotic-exposed snails showed a greater difference in shell thickness between the risk treatments than controls. This was because in the absence of antibiotics, snails formed thick shells even when they experienced only low risk, which is likely the result of infection with unknown pathogens. By eliminating these pathogens, antibiotic treatment uncovered a greater amount of plasticity.

Does that mean that we should always use antibiotics as a prophylactic treatment during future studies? No – because parasites and pathogens are part of nature. If we want to understand if and how animals cope with the presence of predators or other environmental change in their natural environment, we need to consider that it may be common for them to be infected at the same time. Nevertheless, if our research questions are less concerned with the natural circumstances and are more focused on mechanics of plasticity, prophylactic antibiotic use may be quite helpful.

However, not all questions are answered with this study. For example, it remains unknown which specific pathogen or parasite in our snails could have caused them to grow thicker shells. They may do so because thicker shells do not only protect the snails but also their parasites. We know that some flatworms can cause snail shells to grow thicker, but in our study population we can largely exclude their presence. Maybe there are some microbes with similar mechanisms at work? Hopefully, future studies will help us learn more.

Read the paper

Read the full paper here: Meuthen, D. & Reinhold, K. (2023) On the use of antibiotics in plasticity research: gastropod shells unveil a tale of caution. Journal of Animal Ecology, 00: 1-10. https://doi.org/10.1111/1365-2656.13909

About the Author

I am an evolutionary ecologist with a special interest in antipredator phenotypic plasticity, who studies both inducing chemical cues as well as its evolutionary consequences in fish and snails. I also have broad interests in chemical ecology, genetics, visual ecology, toxicology and personality research. I am a disabled scientist ( https://www.nature.com/articles/d41586-022-00230-3 ), currently a Freigeist fellow funded by the Volkswagen Foundation at Bielefeld University in Germany and the principal investigator of the IDEA-Lab (@m_idealab@twitter.com, @idealab@fediscience.org).

Using microclimatic data and niche modeling to predict the daily activity of a desert lizard

This blog post is provided by Felipe A. Toro-Cardona, Juan L. Parra and Octavio R. Rojas-Soto and tells the #StoryBehindthePaper for the paper “Predicting daily activity time through ecological niche modeling and microclimatic data”, which was recently published in Journal of Animal Ecology. In their paper they explore how the Gila monster’s daily activity is impacted by microclimate, and find that daily activity varies between seasons, so traditional methods are not effective models for this species, but using different temporal scale data can help predict daily activity.

This blog post is provided by Felipe A. Toro-Cardona, Juan L. Parra and Octavio R. Rojas-Soto and tells the #StoryBehindthePaper for the paper “Predicting daily activity time through ecological niche modeling and microclimatic data”, which was recently published in Journal of Animal Ecology. In their paper they explore how the Gila monster’s daily activity is impacted by microclimate, and find that daily activity varies between seasons, so traditional methods are not effective models for this species, but using different temporal scale data can help predict daily activity.

All species show a time preference for feeding and breeding; migratory birds usually breed during the spring, some butterflies only feed during their caterpillar phase, and public knowledge tells us that the likelihood of fishing increases at dawn or dusk. Two features that explain these preferences are species’ physiological limits and microclimatic conditions. The activity of the species varies at different temporal scales; but most research has concentrated on annual or seasonal variation.

Temporal patterns of activity have been usually studied between seasons through radio tracked animals, camera traps, or using ecological niche models with monthly resolution. These models relate climatic variables with georeferenced observations of the species to generate a prediction of the suitable environmental conditions for each species. These models are used to study biodiversity in the context of climate change, conservation, and invasions. However, activity patterns are rarely considered.

Our study began using standard methodologies to model the niche of the Gila Monster (Heloderma suspectum) recognizing its seasonal activity pattern. These methods use the month or season in which the species is most active as a reference, assuming that the climate in that moment (year, month, or season) is the most suitable for the species. In this way, a prediction is obtained for each month or season. We made a first approximation for the Gila monster using May as the time of breeding activity. However, this first approximation did not show adequate results since predictions were not accurate for other months (e.g. August).

Example of the result of modeling the Gila Monster using standard methodologies for seasonal species. In this case we observed that projection of the model (training in May) to August had low prediction capacity of the occurrences observed in August.

After a bibliographic review of the ecology of the Gila monster, we found that the species presents hourly activity patterns that vary between seasons. In spring, the species presents a peak of activity in the morning between 9 and noon. In summer, due to the high temperatures, the species altered its activity in two parts, a diurnal one from 8 a.m. to 11 a.m. and a crepuscular/nocturnal one from 4:00 p.m. to 9:00 p.m. Finally, when winter began, its activity decreased considerably, limiting itself to a few hours between 11 am and 1pm. This temporal variation in climate made it difficult to make predictions using previous methods.

Heloderma suspectum (Gila monster). (Photo credit: Paul Maier)

One possible solution to adequately model the niche of the Gila monster, was to consider its daily seasonal pattern of activity. With this purpose in mind, we first obtained all the records of the species. We then divided our data into a training set that included only museum specimens without the time of capture, and a testing set consisting of citizen science observations with the time of each record. For each record, we simulated its microclimate (minimum and maximum temperature and relative humidity at ground level) for each hour of the day throughout a year. Once the microclimate values ​​for each record were obtained, we used the training set to generate the niche models using minimum volume ellipsoids. These ellipsoids represent the microclimatic space used by the Gila monster and may be interpreted as an approximation of its fundamental niche.

Fundamental niche generated with microclimatic data. Black ellipsoid represents niche using May occurrences, while the red one represents the niche considering the hour of activity from May to August

The model generated with the microclimatic data from all activity hours of the different months included 95% of the citizen science records. In contrast, the model with microclimatic data only from May only included 13%. Further, the best model allowed us to recover the spring and winter unimodal pattern of daily activity and a bimodal pattern during the summer. We observed greater microclimatic suitability in the hours of greatest activity reported in previous studies. In addition, the peaks of activity and inactivity are consistent with and may be regulated through the species’ physiological tolerance to high temperatures. In other words, if the weather gets too hot (> 37°C on the ground at a particular time of the day), Gila monsters crawl into their burrows.

We conclude that it is possible to rescue the daily activity patterns at an hourly level with niche models and that the estimation of the niche breadth can vary considerably depending on the temporal resolution of environmental variables used. This has interesting implications and applications for studies of climate change, conservation proposals, and even sampling designs anywhere on the planet.

Read the paper

Read the full paper here: Toro-Cardona, F.A., Parra, J.L. and Rojas-Soto, O.R. (2023), Predicting daily activity time through ecological niche modeling and microclimatic data. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13895

What makes an urban bird?

This blog post is provided by Jenny Ouyang and tells the #StoryBehindthePaper for the paper “Changes in the rearing environment cause reorganization of molecular networks associated with DNA methylation”, which was recently published in Journal of Animal Ecology. In their paper they explore the impact of urbanisation on DNA methylation in young birds.

Urbanization is one of the most prevailing forms of habitat change, causing biodiversity loss through local extinction processes. Urban expansion is expected to impact a quarter of all endangered species in the next decade. Nevertheless, individuals vary in their response to these drastic changes, with some unable to occupy these new habitats while others persist and thrive.

This difference in the ability to adapt has promoted the study of phenotypic traits that allow individuals to inhabit urban areas. A key trait that can facilitate adaptation is the degree at which animals respond to stressors. This stress response, which includes elevation of baseline circulating concentrations of glucocorticoids, has a heritable component and exhibits individual variation. Epigenetic mechanisms can alter organism function without changes in the DNA sequence, representing a possible mechanism for the observed response to urban stressors.

Female house wren at an urban site (Caughlin Ranch) with a caterpillar ready to feed its offspring in the nest box. Photo credit: Michael Dale

In a recent paper in the Journal of Animal Ecology, we explored the contribution of DNA methylation towards observed urban phenotypes. When house wren parents bred in nestboxes across a network of urban and rural field sites, we moved their offspring across and within sites to disentangle the contribution of genetic and plastic mechanisms to the glucocorticoid phenotype. This type of experiment is an inter- and intra-environmental cross-foster to analyze the contribution of DNA methylation to early-life phenotypic variation.

Young house wrens were moved within and among urban and rural sites to investigate the contribution

We observed age-related patterns in offspring methylation, indicating developmental effects of the rearing environment. We further discovered different networks of genes were important at hatching compared to fledging. For example, we found several genes involved in auditory response and learning networks were differentially methylated across experimental treatments. Analyses showed that cellular respiration genes were differentially expressed at hatching and behavioral and metabolism genes were differentially expressed at fledgling. Lastly, hyper-methylation of a single gene (CNTNAP2) is associated with decreased glucocorticoid levels and the rearing environment. Urban house wrens appear to be hypermethylated during hatching compared to their rural counterparts. As offspring aged, wrens that stayed in the same environment increased methylation frequencies but wrens that moved between environments did not show a similar increase. These age and environment-related changes in methylation frequencies suggest that the urban phenotype is a result of both genetic and environmental factors.

Adult house wren at a rural riparian habitat. Photo credit: Chris Halsch.

Our findings are suggestive that DNA methylation can shape the physiological phenotype and is empirical evidence for a mechanism by which individuals thrive in changing environments. Together, this work provides an unprecedented empirical system that we have leveraged to explore the influence of both genetics and environment on DNA methylation. DNA methylation may be a mechanism by which individuals adjust to novel environments during their lifespan. Understanding the genetic and environmental basis of local adaptation is important in predicting species’ responses to an urbanizing world.

Author bio

Jenny Ouyang – I am an integrative physiologist at the University of Nevada, Reno. I am interested in how animals physiologically adapt to changing environmental conditions.

Read the paper

Read the full paper here: von Holdt, B. M., Kartzinel, R. Y., van Oers, K., Verhoeven, K. J. F., & Ouyang, J. Q. (2023). Changes in the rearing environment cause reorganization of molecular networks associated with DNA methylation. Journal of Animal Ecology, 00, 1– 17. https://doi.org/10.1111/1365-2656.13878

Combined analysis of primate and parasite traits reveals new insights on ecological networks

This blog post is provided by James Herrera, Ph.D., Duke Lemur Center SAVA Conservation Initiative and tells the #StoryBehindthePaper for the paper “Predicting primate-parasite associations using exponentional random graph models”, which was recently published in Journal of Animal Ecology. In their paper they show that large primates in warm climates and sharing the same biogeographic region have more parasites than small species in cool, dry climates. Parasites known from multiple non-primate hosts, especially viruses, protozoa, and helminth worms infect more primates than primate-specific parasites or fungi and bacteria. Advanced social network analyses allowed the first multidimensional analysis of primate-parasite ecological interactions.

After three years of the coronavirus pandemic, we have all become keenly aware of the impacts pathogens have on global systems. Parasites are ubiquitous in nature, including all species that live on or inside another organism – the host – from which they get their resources. Wild animals are often co-infected by multiple parasites at the same time. The chimpanzee, for example, is known to host over 100 parasites; chimps are one of the best studied primates because of their close relationship to people and the relevance of chimp parasites for human health. In contrast, species like the indri, a lemur only found on Madagascar, are only known to host about 10 parasites. Many other primates are so poorly studied, only 1 parasite has ever been recorded.

Chimpanzees (left) are one of the best studied primates for parasite interactions. In contrast, the indri (right) is comparatively poorly known for its parasites. (Photo credits: chimpanzee: Wikimedia Commons; indri: James Herrera)

In a new study published in the Journal of Animal Ecology, we examined which traits of both primates and parasites predict the likelihood of their interactions. Using advanced techniques in social network analysis, called the exponential random graph, we were able to simultaneously test the traits of primates and parasites to determine what predisposes primates to infection and what gives some parasites a unique advantage. For primates, larger species that are found in warmer, wetter climates are more likely to host diverse parasites, compared to smaller species living in drier, cooler climates. Further, species in the same branches of the evolutionary tree and those that live in the same geographic region are more likely to share parasites than more distantly related species found on different continents. Viruses, protozoa, and helminth worms are more likely to infect diverse primates than fungi, arthropods, and bacteria. Parasites that are known to infect non-primate mammals are also more likely to infect diverse primates.

A photo from a microscope slide showing the blood parasite Plasmodium falciparum, one of the pathogens that causes malaria, a devastating disease in people, and also infects 118 other primates. In contrast, there are at least 30 other kinds of Plasmodium that only infect one or a few primates and effects on disease are poorly understood. (Photo credit: Wikimedia Commons)

These new results were made possible by the great advances being made in infectious disease ecology. Over the last two decades, Dr. Charles Nunn at Duke University’s Evolutionary Anthropology and Global Health departments has been working with teams of researchers to compile all published records of primate-parasite interactions. Combing through the literature, almost 600 published sources were obtained to glean which parasites are found in over 200 primates species, with over 2,300 interactions recorded. With the analytical tools in social network science mastered by Duke Sociology professor Dr. James Moody, we were able to systematically test how traits of both hosts and parasites affect the likelihood of their interaction for the first time. While many previous studies used subsets of this database and examined either hosts or parasites in isolation, we were able to make new inferences about the critical links in this unique ecological network.

This work builds on a recent study that showed how extinction of primate hosts could lead to the co-extinction of almost 200 parasite species. While at first this might seem like a good thing, in fact it could have negative impacts on biodiversity as a whole. Many parasites don’t actually cause disease or death in the hosts, and some may even have beneficial properties. We simply don’t know enough about these critical and co-evolved relationships to understand what effects host-parasite coextinctions could have in the long-term.

While it might seem strange to worry about parasite extinctions, they are actually an important part of biodiversity and ecosystem functions. Understanding how primates and parasites interact reveals new insights into coevolutionary theory, and could also contribute to the conservation of underappreciated species richness. While from a public health perspective, we’d like to see some parasites disappear, like corona and ebola viruses, from an evolutionary stance, the sheer diversity of parasites and their intimate relationships with their hosts make them fascinating and crucial components of biodiversity.

Read the paper

Read the full paper here: Herrera, J.P., Moody, J. and Nunn, C.L. (2023), Predicting primate-parasite associations using exponentional random graph models. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13883

Ecological patterns and processes in the vertical dimension of terrestrial ecosystems

This blog post is provided by Shuang Xing and tells the #StoryBehindthePaper for the paper “Ecological patterns and processes in the vertical dimension of terrestrial ecosystems”, which was recently published in Journal of Animal Ecology. In their paper they explore how forests show ecological patterns from forest floor to canopy.


The vertical structures of terrestrial vegetation provide important habitats for diverse forms of life to occur, disperse and reproduce.   From the ground to the forest top, the changes in resources, microclimate, and habitat structure create a complex combination of environmental gradients within a short spatial distance. In this review, we explore the ecological evidence that the vertical gradient is an influential engine driving the ecology and evolution of forest species, shaping larger biogeographic patterns in space and time.

Ecological patterns in the vertical dimension
Figure 1. Vertical structure in (A) temperate forest and (B) tropical forest. Photo credit: (A) Shuang Xing, (B) Xinyue Chang

Evidence from different taxa and ecosystems shows that the forest ecosystem is a three-dimensional realm, allowing species to move, adjust and select their favourite microhabitat horizontally and vertically.  The architecture of the tree crown and the profile of foliage, together with the tree’s height, provide a high heterogeneity of vertical environment for arboreal biota (Fig. 1). The forest layers and vertical distance generate a climatic gradient from the ground to the canopy. In general, the canopy microclimate is drier, warmer, and more variable than the understory.  As such, the arboreal distribution of species can be uneven, resulting in vertical stratification patterns observed from different groups of animals. The interplay between variances in microclimate, resources and vegetation structure along the vertical gradient can affect the vertical distribution of species, and may further shape the distribution of species at larger spatial scale. Accordingly, the vertical distribution of species can change at different time scales from daily to annually, depending on the changing rate of critical environmental factors and the life history of the organisms involved. In addition, the vertical niche of a species can be further refined by species interactions, spanning within trophic levels such as competition, and across trophic levels including parasitism, predation, herbivory, pollination, and frugivory.

Ecological mechanisms in the vertical dimension
Figure 2. A hypothetical community assembly showcasing ecological processes through which abiotic and biotic factors in combination with species traits and biotic interactions sorts a neutral species pool into vertically partitioned communities in space. Illustrated by Laura Corillon and Runxi Wang.

Species have developed multiple mechanisms to adapt to living conditions at certain vertical strata. We grouped them into three main categories: climatic adaptation, dispersal capacity, and specialised life history (Fig. 2). With changes in microclimate from the ground to the canopy, the physiology, morphology, and behaviour of organisms can also vary to adapt to those changes. For instance, canopy species tend to have a broader physiological tolerance for living with highly variable environmental conditions than ground-dwelling species. Vertical differences in climatic-related morphological traits such as body size and body colour have also been observed in animals such as frogs and ants. To overcome the challenges of moving vertically, the movement of many arboreal animals involves aerial behaviours such as flying, parachuting, and gliding.  For instance, some mammals and reptiles such as Belomys pearsonii Gray (see Fig. 3 below) and Chrysopelea ornate (see Fig. 4 below) move across tree crowns by gliding. For tree frogs like Rhacophorus dennysi (see Fig. 5 below), the adhesive toe pads can help them to grip and attach on the smooth surface of leaves and branches.  Some species “migrate” from the ground to the canopy within their life cycle and make full use of different microhabitats and microclimatic conditions provided by vertical tree structures.

Figure 3. Belomys pearsonii Gray eating fruits in a tropical rainforest. Photo credit: Wenda Cheng
Figure 4. Chrysopelea ornate in the canopy. Photo credit: Wenda Cheng
Figure 5. Rhacophorus dennysi and its vertical habitat. Photo credit: Wenda Cheng
Future directions

We encourage ecologists to acknowledge and embrace the multidimensionality of ecosystems and test ecological theories within and beyond the vertical dimension. We suggest that only by including the patterns, processes, and mechanisms in the vertical dimension in addition to those in the horizontal dimension, can we have a complete understanding of the mechanisms underlying current biodiversity distribution, and how these may respond to global changes.

About the author

I am Shuang Xing, an assistant professor at the Sun Yat-sen University. I study how species and ecological networks respond to environmental changes. I aim to understand the vulnerability of species and ecosystems to multiple threats, including climate change, deforestation, and wildlife trade.

Twitter account: @ShannonXing

Read the paper

Read the full paper here: Xing, S., Leahy, L., Ashton, L. A., Kitching, R. L., Bonebrake, T. C., & Scheffers, B. R. (2023). Ecological patterns and processes in the vertical dimension of terrestrial ecosystems. Journal of Animal Ecology, 00, 1– 14. https://doi.org/10.1111/1365-2656.13881


这篇博文由邢爽提供,讲述了其最近发表在《Journal of Animal Ecology》上的论文“Ecological patterns and processes in the vertical dimension of terrestrial ecosystems” #文章背后的故事。在这篇论文中,作者们探讨了森林中从地面到林冠所呈现的生态格局。

Read the blog in English here.



在不同类群和生态系统中,森林生态系统都是一个三维的空间系统,支持物种在水平和垂直空间中移动、调整并选择他们最适合的微生境。树冠和枝叶的形态结构与树的高度共同为树栖生物提供了具有高度异质性的垂直环境 (图一)。同时,不同林层及从地面到林冠的垂直距离塑造了气候梯度。总体上,林冠的微气候相比于林下更加干燥、温暖和多变。因此,树栖物种的分布并不均匀,在不同动物类群中展现出垂直分层格局。在垂直梯度下的微气候、食物资源和植被结构及其交互作用的变化共同影响了物种的垂直分布,并可能进一步在大空间尺度上塑造物种分布格局。与此同时,物种的垂直分布也由于关键环境因素和自身生活史的影响从日间到年间在不同时间尺度上发生变化。除此之外,物种的垂直生态位也会受到包括同一营养级之间的竞争,及跨营养级的寄生、捕食、植食、传粉和食果等物种间相互作用的限制。


物种为适应不同垂直分层的生存环境形成了多种机制。我们将这些适应机制归纳为以下三类:气候适应、扩散能力和特化的生活史 (图二)。随着从地面到林冠的微气候变化,生物的生理、形态和行为会随之变化以适应环境。比如,相较于地面栖息的物种,林冠物种趋向有较广的生理耐受度。并且与气候适应相关的形态特征,比如体型和体色,也在一些动物类群(如:蚁类和蛙类)中呈现出了垂直差异性。为了克服在垂直方向移动的挑战,许多树栖动物演化出了包括飞行、降落和滑翔等在空中移动的行为。一些哺乳动物和爬行类如毛耳飞鼠(Belomys pearsonii Gray,见图三)和金花蛇(Chrysopelea ornate,见图四)利用滑翔在树冠间移动。而对于像大树蛙Rhacophorus dennysi (见图五)这样的树栖蛙类,趾端的吸盘结构可以帮助它们抓握和附着于光滑的叶片和树枝表面。一些物种在其生活史中,会通过在地面和林冠之间 “迁移”来利用垂直结构中不同的微生境和微气候条件。

图二. 以一个假设的群落集合为例,演示不同环境与生物因素通过物种生态机制和种间相互作用塑造物种垂直分布格局的生态过程。 插图设计者为Laura Corillon和王润玺。
图三. 毛耳飞鼠(Belomys pearsonii Gray)在热带雨林中取食树上的果子。图片来源: 程文达
图四. 林冠上的金花蛇(Chrysopelea ornate)。图片来源:程文达
图五. 大树蛙 (Rhacophorus dennysi) 和它的垂直栖息地。图片来源:程文达





Ants don’t change their behavior to avoid sublethal warming

This blog post is provided by Elsa Youngsteadt and tells the #StoryBehindthePaper for the paper “Can behavior and physiology mitigate effects of warming on ectotherms? A test in urban ants”, which was recently published in Journal of Animal Ecology. In their paper they explore how ants might react to climate change, and whether they can adapt their behaviour to new conditions.

Spring flowers are bursting earlier, growing zones are marching ever poleward, and bumble bees are shrinking away from their southern range limits. Climate change is well underway and some of its biological effects have been established for decades. But other effects are more subtle. For example, physiologists predict that, as temperatures increase, some animals’ metabolisms will also ramp up. They’ll need more food to get by, they’ll live faster, and die younger; some will go extinct. But are animals really getting hotter as the climate warms up?

Ectotherms are animals that don’t maintain a constant body temperature, instead letting it fluctuate along with the environment. But they do exert some control, for example by moving between sun and shade or retreating underground at certain times of the day or year. Given this ability to thermoregulate, ectotherms might also buffer their own exposure to climate change by subtly shifting their activity to cooler microclimates within their habitat. Although some modeling studies have suggested that this ability would save many insects from heat-induced extinction, it’s not clear that they really have the behavioral flexibility to pull it off. This is one of the main questions my team and I had heading into the spring of 2020.

Of course, the spring of 2020 didn’t go as planned. We had meant to ask this question in the warm tropics, where ectotherms are closer to their maximum heat tolerance and may take more urgent measures to stave off heat stress. But instead of spending the spring in the tropics, we spent it in lockdown, trying to stay sane and figure out some justifiable use of our time. Once we began to creep back into public, we decided to pilot our tropical methods at home in Raleigh, NC. That pilot project never made it out of the temperate zone, but it did get bigger. Ultimately, we found that our own local ants—although not obviously heat stressed—are surely warming up.

Checking for ants during a nighttime transect survey. Photo credit: Sara Prado

To detect behavioral thermoregulation, it’s not enough to just measure an ectotherm’s body temperature. You need to know its preferred body temperature, and what range of temperatures are available in its habitat—in the thermal mosaic created by shade, sun, darker surfaces, lighter surfaces, and little breezes. With those pieces of information, you can see how challenging the thermal environment actually is. (If the animal moved carelessly through the habitat, would it ever encounter intolerable conditions, or only pleasant ones?) And even if no part of the environment is truly pleasant, you can see whether the animal is making the best of it, spending time in the microclimates that bring it closest to its preferred temperatures, even if it’s still way off.

We chose ants as our focal ectotherms because they’re common models for thermal biology research, and because they’re generally important participants in their ecosystems, acting as predators, herbivores, seed dispersers, and so on. To look at a climatic challenge to ant thermoregulation, we worked on an urban warming gradient. All our sites were forested, but the ones located along urban greenways averaged about one degree Celsius warmer in the summer than the non-urban forest sites.

Map and examples of study sites. All sites were forested, but some were hotter than others due to their location within the urban heat island of Raleigh, NC.

We worked with several ant species that were common across most of the study sites, and collected four kinds of data. First, we measured thermal preference—the range of temperatures where each species chose to settle on a gradient from a heat block to an ice bath. (Because the university was still closed, I did this assay in my home office using an apparatus my husband helped build during lockdown. The frozen bowl of our ice cream maker helped keep the cold end cold.) We also measured each species’ maximum heat tolerance. (Sarah Ferriter, an undergrad researcher, took ants to her apartment for this assay.) And finally, research associate Sara Prado measured available and occupied temperatures along transects at each site in the field. For these last two, Sara used operative temperature models of three focal ant species; these were dead, posed ants mounted on thermocouple probes. You can think of them a little bit like a species-specific heat index thermometer: they incorporate effects of air temperature, surface temperature, solar radiation and wind, as well as the size, shape, and color of the ant species. It doesn’t necessarily tell you the body temperature of live ants, but it tells you how comfortable the thermal environment is. If the operative temperature model is hotter than the live ant prefers, then the live ant shouldn’t just hang out in that spot until her own body reaches that unpleasant temperature; she should move along and find some shade.

Operative temperature thermometer for the chestnut carpenter ant (Camponotus castaneus), made from a posed ant specimen (not alive) mounted on a thermocouple temperature sensor. Photo credit: Elsa Youngsteadt
Thermal preference arena. The lanes of the arena span a hot plate and an ice bath; ants indicated their thermal preferences by choosing where to settle within that range. Photo credit: Elsa Youngsteadt

If ants are actually good thermoregulators, then we should find them disproportionately often at places and times where the operative temperatures most closely matched their preferred temperatures. This was the case for four of our five focal species. (The fifth had such a broad range of preferred temperatures that we could hardly ask the question.) But if ants were capable of saving themselves from climate warming by shifting their activity patterns, they should also occupy cooler parts of the transect at sites that were too hot, and hotter parts of the transect at sites that were too cool. This did not happen. Cool-loving ants, for example seemed to use fixed behaviors (like being more active at night) to avoid the hottest conditions across the board—even at sites where the temperature was more comfortable during the day.

Black field ants (Formica subsericea) at a bait station. Ants were only slightly more likely to use a bait station if it was placed in a preferred microclimate than if it was placed in an uncomfortable microclimate that was too hot or too cold. Photo credit: Sara Prado

None of the ants got dangerously hot or cold during our study. But they did get warmer than they preferred to be, and they didn’t shift their behavior to compensate. That means urban ants are hotter than non-urban ants, and as climate change progresses, future ants will probably be hotter than past ants. If this pattern holds, their metabolisms will increase, and they’ll live faster-paced lives. Because ants are social animals, the bottom line for the superorganism—as opposed to just its individual workers—is still unknown. That’s something we’d like to know next. Only this time, I hope it doesn’t take a pandemic to send us back out to our local field sites to find out. 

Author bio

Elsa Youngsteadt is an assistant professor in the Department of Applied Ecology at North Carolina State University.

Lab website: http://youngsteadtlab.org/

Read the paper

Read the full paper here: Youngsteadt, E., Prado, S. G., Keleher, K. J., & Kirchner, M. (2022). Can behaviour and physiology mitigate effects of warming on ectotherms? A test in urban ants. Journal of Animal Ecology, 00, 1– 12. https://doi.org/10.1111/1365-2656.13860

Systemic pathogens and coinfection associate with changes in the gut microbiota of bank voles 

This blog post is provided by Ilze Brila and tells the #StoryBehindthePaper for the paper “Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole (Myodes glareolus”, which was recently published in Journal of Animal Ecology. In their paper they explore how coinfection of pathogens impact the microbiota of bank voles.

Bloga ierakstu angliski iespējams lasīt šeit.

Gut microbiota is the collection of microorganisms (such as bacteria and microfungi) inhabiting the gastrointestinal tract of an animal. The gut microbiota provides many important functions and services to its host and is, therefore, a crucial part of animal physiology and health. It is thus unsurprising, that the number of studies examining factors affecting gut microbiota has skyrocketed in recent years to demonstrate how the gut microbiota can be affected by diverse features of the host and its environment, including infection by pathogens. 

Wild animals can be infected by a variety of pathogens, both macroscopic such as helminths, and microscopic, such as protozoans or bacteria. The possibility of interactions between gastrointestinal pathogens and the gut microbiota might seem obvious, as both the parasite and the microbiota inhabit the same environment. But one unresolved question is whether infection by systemic pathogens (those found in blood or multiple tissues) is associated with changes in the gut microbiota of wild animals. Importantly, coinfections (infections by multiple pathogens simultaneously) are the norm in nature, and it is, therefore, essential to understand whether coinfections would affect the pattern of the pathogen-microbiota interactions.

To answer these questions, we determined whether bank voles (Myodes glareolus) were infected by four systemic pathogens: Puumala orthohantavirus, apicomplexan protozoan Babesia microti, and the bacteria Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato. We investigated the gut microbiota – systemic pathogen relationships by asking (1) whether the effects of systemic pathogens depend on the pathogen’s identity and/or whether they affected by coinfections and (2) whether the effects of coinfection (compared to a single infection) on gut microbiota are similar for all pathogens. In short, the respective answers to our questions are “yes”, and “no”. Let me dive into the details. 

A juvenile bank vole (Myodes glareolus) in Finland (Photo credit: Ilze Brila)

Out of the 67 voles that were infected with any of the four pathogens, 36 were coinfected, with a high number of different coinfections – we detected 9 types of coinfections out of the 11 possible combinations of coinfection. Clearly, coinfection is commonplace in nature. This diversity of different coinfections, unfortunately, prevented us from examining the effects of specific coinfections. However, one of the strengths of our work is the ability to compare associations between each pathogen and the gut microbiota when the coinfection status of the animal is overlooked versus the case when coinfection is considered. Do the associations found between pathogens and the gut microbiota stand true after controlling for effects of coinfection? 

While each pathogen indeed had a unique association with the gut microbiota of bank voles, we found that only Anaplasma phagocytophilum had the same association with gut microbiota ß-diversity (between-sample diversity) regardless of whether the coinfection status is overlooked or considered. For the other three pathogens, overlooking coinfection status led to misleading conclusions on the pathogen-microbiota associations in a pathogen-specific way. 

How did the effects of a pathogen differ in a single-infection vs coinfection scenario? To answer this question, we used a framework outlined by Schmid et al. to compare the effects of coinfection with those of a single pathogen infection for each pathogen. In brief, we focussed on identifying whether the effects of a coinfection when compared to those of a single infection are best described as a) synergistic, whereby the effects of a pathogen are exacerbated by coinfection, b) neutral, when there is no significant difference between single infection versus coinfection scenarios, and c) antagonistic, where coinfection apparently counteracts the effects of a single pathogen infection. We uncovered evidence for all three possible effects of coinfection, with antagonistic effects occurring more often. The type of effect of coinfection was, again, dependent on the pathogen identity. Moreover, the impacts of coinfection also depended on the type of metric used to characterise variation in the gut microbiota community, potentially indicating infection-specific impacts on the rare or abundant gut bacteria. 

So, what are the take-home messages from our article? We show that overlooking coinfections can affect the pattern of pathogen-microbiota associations. We, therefore, encourage future studies to examine a wider diversity of pathogens relevant to study species in the specific region to better account for this apparent effect of coinfection. This, of course, will not be easy, given the potentially large number of pathogens that may (co)infect an animal, and the difficulties of pathogen screening in wildlife. Yet we believe that acknowledging infection heterogeneity (the number of concurrent infections and infection length or sequence) present in wild animal populations will provide interesting insights and lead to a better understanding of the complex interactions between hosts, their pathogens, and the gut microbiota. This in turn could provide a better understanding of how these multi-directional relationships may affect host health and disease dynamics in wild animals. 

Overview of the study. We used wild bank voles as a model organism to examine the association between the gut microbiota and four systemic pathogens. We examined whether 1) the effects of coinfection generally differ from those of a single infection, 2) the effects of the four pathogens differ and 3) the effects of a specific pathogen differ depending on the coinfection status of the animal (Credit: Ilze Brila, with help from Māris Grunskis)

A few final notes for those who have made it to (or scrolled down to) the end of this blog post. I am grateful for the constructive comments of all reviewers and the editor during the review process. However, I am especially grateful for one reviewer, whose detailed, constructive, and encouraging comments considerably improved the manuscript and were greatly appreciated by an early career researcher such as myself. Thank you. Another note I want to add is that all of our sequencing data, as well as metadata and code, are publicly available in NCBI SRA and Figshare. So, if reading our paper makes you want to dig a little bit deeper – please do! None of this work would have been possible without the community of researchers who make their analysis and code freely available. If you can repay this help by sharing your code, I encourage you to do so. 

Read the paper

Read the paper here: Brila, I., Lavrinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T., & Watts, P. C. (2022). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole Myodes glareolusJournal of Animal Ecology, 00, 1– 12. https://doi.org/10.1111/1365-2656.13869

Sistēmiskie patogēni un koinfekcijas ir saistītas ar izmaiņām rūsgano mežstrupastu zarnu mikrobiotā

Šī bloga ieraksta autore ir Ilze Brila, un tas ir stāsts par (#StoryBehindthePaper) publikāciju “Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole (Myodes glareolus”, kas nesen publicēts žurnālā Journal of Animal Ecology. Publikācijas autori pēta kā patogēnu infekcijas un koinfekcijas ietekmē rūsgano mežstrupastu zarnu mikrobiotu.

Read the blog in English here

Zarnu mikrobiota ir gremošanas traktā mītošo mikroorganismu, piemēram, baktēriju un sēnīšu, kopums vai sabiedrība (nejaukt ar zarnu mikrobiomu). Zarnu mikrobiota pilda daudzas dzīvnieku fizioloģijai un veselībai kritiski svarīgas funkcijas. Tādēļ nav pārsteidzoši, ka pēdējos gados ir strauji pieaudzis to ietekmējošo faktoru pētījumu skaits, kuri parāda, ka zarnu mikrobiotu ietekmē dažādi saimniekorganisma un vides faktori, kā arī patogēni, ar kuriem dzīvnieks inficēts.

Savvaļas dzīvnieki var būt inficēti ar visdažādākajiem patogēniem – gan makroskopiskiem, piemēram, helmintiem (parazītiskiem tārpiem), gan mikroskopiskiem, piemēram, baktērijām un vienšūņiem. Mijiedarbība starp zarnu patogēniem un zarnu mikrobiotu varētu šķist likumsakarīga, tā kā abi dzīvo vienā vidē. Tomēr nav līdz galam skaidrs, vai sistēmiskie patogēni (tie, kas sastopami asinīs vai vairākos audos) spēj mijiedarboties ar zarnu mikrobiotu. Turklāt savvaļas dzīvnieki bieži ir inficēti ar vairākiem patogēniem vienlaikus (koinficēti), tādēļ rodas jautājums, vai koinfekcijas var ietekmēt mijiedarbību starp patogēniem un zarnu mikrobiotu. Nesen publicētajā rakstā mēs mēģinājām rast atbildes uz abiem šiem jautājumiem.

Mēs noteicām, vai rūsganās mežstrupastes (Myodes glareolus) ir inficētas ar četriem patogēniem – baktērijām Anaplasma phagocytophilum un Borrelia burgdorferi sensu lato, vienšūņiem Babesia microti un Puumala Ortohanta vīrusu. Mēs jautājām (1), vai sistēmisko patogēnu ietekme uz zarnu (bakteriālo) mikrobiotu atkarīga no patogēna identitātes un vai to ietekmē koinfekcijas, un (2) vai koinfekcijas efekti (salīdzinot ar viena patogēna infekcijas efektiem) ir vienādi visiem patogēniem. Īsumā, atbildes ir “jā” un “nē’’.

Jauns rūsganās mežstrupastes (Myodes glareolus) īpatnis Somijā (Ilze Brila)

No 67 mežstrupastēm, kuras bija inficētas ar vismaz vienu patogēnu, 36 bija koinficētas ar lielu skaitu dažādu koinfekciju – mēs konstatējām 9 no 11 iespējamajām koinfekcijām, vēlreiz apliecinot to, ka koinfekcijas dabā ir plaši izplatītas. Ņemot vērā lielo skaitu dažādo koinfekciju, mēs nevarējām analizēt specifiskas koinfekcijas. Taču viena no mūsu pētījuma stiprajām pusēm ir iespēja salīdzināt katra patogēna mijiedarbību ar zarnu mikrobiotu gadījumos, kad koinfekcijas tiek ņemtas un kad tās netiek ņemtas vērā. Tādējādi mēs varam izpētīt, vai atklātās asociācijas starp patogēnu un zarnu mikrobiotu ir patiesas neatkarīgi no koinfekcijām.

Lai arī katra patogēna attiecības ar zarnu mikrobiotu bija unikālas, tikai Anaplasma phagocytophilum attiecības ar zarnu mikrobiotas ß-daudzveidību (starpindivīdu daudzveidību) bija nemainīgas, ņemot vai neņemot vērā koinfekciju status. Pārējo patogēnu gadījumā, ja koinfekcijas netika ņemtas vērā, mūsu secinājumi par patogēnu un zarnu mikrobiotas attiecībām bija neprecīzi, turklāt katram patogēnam specifiskā veidā.

Kā patogēna ietekme uz zarnu mikrobiotu atšķīrās viena patogēna infekcijas vai koinfekcijas gadījumā? Lai atbildētu uz šo jautājumu, mēs izmantojām Schmid et al. pētījumu, lai salīdzinātu koinfekcijas efektus ar viena patogēna infekcijas efektiem katram patogēnam. Īsumā, koinfekcijas efekti var tikt uzskatīti par a) sinerģiskiem, ja patogēna ietekme uz zarnu mikrobiotu ir saasināta koinfekcijas gadījumā, b) neitrāliem, ja efekti vienas infekcijas vai koinfekcijas gadījumā neatšķiras, vai c) antagonistiskiem, ja koinfekcija darbojas pretī viena patogēna efektiem. Mūsu pētījumā mēs novērojām visus trīs iespējamos koinfekcijas efektus, lai gan antagonistiski efekti bija sastopami visbiežāk. Arī koinfekcijas efekti (salīdzinot ar viena patogēna infekcijas efektiem) bija atkarīgi no konkrētā patogēna. Tāpat mēs novērojām atkarību no izmantotā ß-daudzveidības mērījuma – vai tie labāk uzsver efektus uz bieži vai reti sastopamām zarnu baktērijām.

Tad kādi ir mūsu galvenie secinājumi, kurus vērts atcerēties? Mūsu pētījums parāda, ka dzīvnieka koinfekciju neņemšana vērā var ietekmēt patogēna un zarnu mikrobiotas attiecību novērojumus. Tādēļ mēs mudinām tālākos pētījumos iespēju robežās ņemt vērā patogēnus, kas sastopami konkrētajā sugā un ģeogrāfiskajā reģionā. Protams, ka tas nebūs viegli, ņemot vērā lielo skaitu dažādo patogēnu, ar kuriem dzīvnieks var būt inficēts, kā arī savvaļas dzīvnieku patogēnu pētījumu sarežģītību, taču mēs uzskatām, ka pētījumi, kas ņems vērā savvaļas dzīvniekos sastopamo infekciju neviendabīgumu (piemēram, vienlaicīgu infekciju skaitu, infekcijas ilgumu vai infekciju secību), sniegs aizraujošu ieskatu un ļaus mums labāk izprast sarežģītās saimniekorganisma, zarnu mikrobiotas un patogēnu mijiedarbību. Šī izpratne, savukārt, ļaus labāk saprast, kā šī mijiedarbība var ietekmēt savvaļas dzīvnieku veselību un slimības.

Pētījuma pārskats. Izmantojot rūsganās mežstrupastes kā modeļorganismu, mēs pētījām saistību starp zarnu mikrobiotu un četriem sistēmiskiem patogēniem. Konkrētāk, mēs pētījām, vai 1) koinfekcijas efekti vispārīgi atšķiras no vienas infekcijas efektiem, 2) četru pētīto patogēnu efekti ir vienādi un 3) konkrētā patogēna ietekme uz zarnu mikrobiotu ir atkarīga no dzīvnieka koinficēšanās stāvokļa. (Ilze Brila & Māris Grunskis)

Daži pēdējie komentāri lasītājiem, kas nonākuši līdz ieraksta beigām. Šī raksta recenzentu un redaktora darbs bija ievērojams un būtiski uzlaboja mūsu publikāciju. Esmu īpaši pateicīga vienam no recenzentiem, kura/-s rūpīgie, vērtīgie un atbalstošie komentāri bija ļoti noderīgi un novērtēti. Paldies. Vēl viena lieta, kuru vēlos izcelt – visi mūsu dati ir brīvi pieejami NCBI SRA un Figshare platformās, tādēļ, ja pēc raksta izlasīšanas jums rodas interese izpētīt ko sīkāk – lūdzu dariet to! Mēs esam publiskojuši arī visu datu analīzei izmantoto kodu vietnē Figshare. Šis raksts nebūtu iespējams bez zinātnieku kopienas, kas padara savu datu analīzi un tajā izmantoto kodu brīvu pieejamu citiem. Ja Jums ir iespēja atmaksāt, daloties ar savu kodu – es Jūs rosinu to darīt!

Izlasi papīru

Izlasi papīru: Brila, I., Lavrinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T., & Watts, P. C. (2022). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole Myodes glareolusJournal of Animal Ecology, 00, 1– 12. https://doi.org/10.1111/1365-2656.13869