Warming and trophic downgrading impact multiple trophic groups within and across ecosystems

This blog post is provided by Pablo Augusto P. Antiqueira. Pablo is a shortlisted candidate for the 2023 Elton Prize, for work on Warming and top predator loss drive direct and indirect effects on multiple trophic groups within and across ecosystems.

This blog post is also available in Portuguese.

The current era is profoundly marked by anthropogenic changes, causing ecological and geological alterations. High species extinction rates and climate change are among the main anthropic consequences that harm and modify ecosystems. Warming, for example, predicted for the following decades, may directly affect biodiversity due to the physiological limitations of organisms or through changes in trophic relationships (e.g., predator-prey interactions), altering the patterns of species diversity and ecosystem functioning. However, some important biological groups, such as predators, may be more sensitive to these impacts, and their extinctions can reorganize or rewire the food web interactions with a variety of cascading indirect effects on the ecosystem functioning.

Considering that the flow of matter and energy connect ecosystems, often through organisms that move between different compartments, anthropogenic effects can propagate between multiple trophic levels within and across ecosystems. For example, changes in aquatic ecosystems can affect aquatic species of different trophic levels, as well as the interaction between them. In addition, many aquatic organisms (e.g., insects) have complex life cycles, with an aquatic larval phase and a terrestrial adult phase – and any alterations in the aquatic ecosystem may decrease or increase the emergence of these organisms to the terrestrial ecosystem, thus affecting terrestrial consumers that feed on them (e.g., spiders and ants). Therefore, anthropogenic changes may be more intense than previously thought, with direct and indirect effects that extend to multiple trophic levels within and across ecosystems.

Freshwater environments are susceptible to climate change and biodiversity loss, with high species extinction rates. Given this scenario, there is a critical need for studies that empirically and objectively address the effect of environmental and biotic changes on biodiversity in freshwater systems and their connection with terrestrial ecosystems. However, one of the significant limitations of carrying out empirical studies on the impact of climate change on ecosystems is the difficulty of conducting field experiments (i.e., realistically) while identifying the ecological mechanisms that occur in the system. Tank-bromeliads (Bromeliacea), an almost exclusively neotropical plant, are naturally well-suited micro ecosystems for such investigations as they support a rich fauna of micro-organisms (e.g., bacteria, algae, fungi, and microfauna) and metazoans (multiple groups of invertebrates, mainly arthropods) in a detritus-based food web (Figure 1). Furthermore, tank-bromeliads are composed of two different compartments—the aquatic and terrestrial —which are interconnected by insect emergence used as resources by various terrestrial predators with varying strategies of hunting that use bromeliads as foraging sites (e.g., cursorial and web-building spiders, ants, centipedes) (Figure 1). 

Figure 1. Illustration of the tank-bromeliad ecosystem (Neoregelia johannis) showing its aquatic and terrestrial compartments, inhabited by a high diverse of macro- and micro-organisms from multiple biological and trophic groups: (i) aquatic microfauna, (ii) aquatic macrofauna and (iii) terrestrial predators (terrestrial macrofauna).

Our study evaluated experimentally, using tank bromeliads as a study system (Figure 2), how the increase in temperature, predicted for the following decades, and trophic downgrading caused by top predator losses, affect the trophic relationships in three connected compartments of the food web: i) aquatic microbiota (algae, ciliates, flagellates, and zooplankton), ii) aquatic macro-organisms (macroinvertebrates) and iii) multiple terrestrial predators from different functional groups, from more active (cursorial spiders and ants) to stationary ones (e.g., web-building spiders). We found that impacts of warming and trophic downgrading on each aquatic (macro and microorganisms) and terrestrial food web compartments depended on the functional group, trophic level, and the community component investigated, i.e., abundance or richness. 

Figure 2. Images from top left to bottom right: 1. Pablo Antiqueira sampling water from tank-bromeliad to evaluate communities of aquatic microfauna and algae community. Photo credits: Gustavo Migliorini. 2-5. Experimental bromeliads in an Atlantic Rainforest understorey, as well as the details of tank-bromeliad top view and the aquarium heaters and temperature sensor inside the tanks. Photo credits: Pablo Antiqueira. 6. A damselfly larva (Leptagrion andromache), a top predator inhabiting tank-bromeliad ecosystem, preying on a beetle larva (Scirtidae, a common detritivore group inhabiting this ecosystem). Photo creditz: Pablo Antiqueira

The trophic downgrading substantially impacted all three compartments of the food web. In the aquatic macrofauna compartment, trophic downgrading increased the richness and abundance of filter-feeding organisms (mosquito larvae – Culicidae), directly and indirectly, through increased detritivore richness, probably through a facilitative interaction. For example, detritivore activity generates fine particles of organic matter, feces, and microorganisms that feed on this material, which filter feeders consume. Thus, the increase in aquatic detritivores after the extinction of top predators also benefited filter-feeding organisms, increasing their richness and abundance. On the other hand, the trophic downgrading decreased algal richness in the microfauna compartment by decreasing nutrient input from the predators’ biological activities (e.g., feces and prey carcasses).

Furthermore, the increase in aquatic filter feeders due to trophic downgrading triggered an increase in terrestrial predators through a cascade effect across ecosystems. The more active terrestrial predators responded more to aquatic trophic downgrading via an increase in the macrofauna species richness than more stationary terrestrial predators. Warming did not affect aquatic micro-organisms or macro-organisms but increased the abundance of web-building terrestrial predators. Our results provide novel evidence on how warming and trophic downgrading can affect the food web of macro- and micro-organisms, not only in the aquatic ecosystem but also in the adjacent terrestrial ecosystem through cross-ecosystem effects.

About the Author

Pablo is an ecologist interested in the factors that regulate community structure and ecosystem functioning. Pablo’s research aims to further understanding of how critical elements of global change alter biodiversity and ecosystem functioning. Pablo is a postdoctoral researcher in the Animal biology department at the University of Campinas (Unicamp), Brazil. @Pablo Antiqueira

O aquecimento e perda de predadores de topo afetam múltiplos grupos tróficos dentro e entre os ecossistemas

Esta postagem no blog é fornecida por Pablo Augusto P. Antiqueira. Pablo é um candidato pré-selecionado para o Prêmio Elton de 2023, pelo trabalho: Aquecimento e os efeitos diretos e indiretos da perda de predadores de topo em vários grupos tróficos dentro e através dos ecossistemas.

A era atual está profundamente marcada por alterações causadas por forças antropogênicas severas, provocando alterações ecológicas e geológicas evidentes. As altas taxas de extinção de espécies e mudanças no clima estão entre as principais consequências antrópicas que agridem e modificam os ecossistemas. O aquecimento, por exemplo, predito para as próximas décadas, pode afetar diretamente a biodiversidade devido às limitações fisiológicas dos organismos ou através de alterações nas relações tróficas (e.g., interações predador-presa), alterando os padrões de diversidade local e regional das espécies além do funcionamento de ecossistemas.  Entretanto, alguns grupos biológicos chaves, como predadores, podem ser mais sensíveis a esses impactos, e suas extinções podem reorganizar ou reconectar as interações da cadeia alimentar com uma variedade de efeitos indiretos em cascata no funcionamento do ecossistema.

Considerando que os ecossistemas estão conectados pelo fluxo de matéria e energia, muitas vezes através de organismos que transitam entre os diferentes compartimentos, os efeitos antropogênicos podem se propagar entre os múltiplos níveis tróficos, dentro e entre ecossistemas. Por exemplo, mudanças nos ecossistemas aquáticos podem afetar as espécies aquáticas de diferentes níveis tróficos, bem como a interação entre eles. Além disso, como muitos organismos aquáticos (e.g., insetos), possuem ciclo de vida complexo, com fase larval aquática e adulta terrestre, tais alterações no ecossistema aquático podem diminuir ou aumentar a emergência desses organismos para o ecossistema terrestre, o que afetaria os consumidores terrestres que se alimentam desses insetos (e.g., aranhas e formigas). Assim, as alterações antropogênicas podem ser mais intensas do que se imaginava, com efeitos diretos e indiretos que se estendem a múltiplos níveis tróficos dentro e entre ecossistemas.

Ambientes de água doce são sensíveis às alterações climáticas e perda de biodiversidade, além de possuírem alta diversidade e altas taxas de extinção de espécies.  Diante desse cenário, é crítica a necessidade de estudos que abordem, de maneira empírica e objetiva, o efeito das alterações ambientais e bióticas na biodiversidade em sistemas de água doce, e sua conexão com sistemas terrestres. Uma das grandes limitações da realização de estudos empíricos sobre o impacto das mudanças climáticas nos ecossistemas é a dificuldade de conduzir a experimentação em campo (i.e., com realismo), ao mesmo tempo em que seja possível a identificação dos mecanismos ecológicos que ocorrem no sistema. As bromélias-tanque (Bromeliacea), uma planta quase exclusivamente neotropical, são microecossistemas naturalmente adequados para tais investigações, pois suportam uma rica fauna de microrganismos (por exemplo, bactérias, algas, fungos e microfauna) e metazoários (vários grupos de invertebrados, principalmente artrópodes) em uma teia alimentar baseada em detritos. Além disso, as bromélias-tanque são compostas por dois compartimentos diferentes – o aquático e o terrestre – que são interligados pela emergência de insetos, que por sua vez são utilizados como recursos por vários predadores terrestres com estratégias variadas de caça (por exemplo, aranhas cursoriais e construtoras de teia, formigas, centopéias) (Figura 1).

Figura 1. Ilustração do ecossistema de uma bromélia-tanque (Neoregelia johannis) mostrando seus compartimentos aquático e terrestre, habitados por uma grande diversidade de macro e microrganismos de múltiplos grupos biológicos e níveis tróficos: (i) microfauna aquática, (ii) macrofauna aquática e ( iii) predadores terrestres (macrofauna terrestre).

Nosso estudo avaliou experimentalmente, utilizando bromélias-tanque como sistema de estudo (Figura 2), como o aumento na temperatura, previsto para as próximas décadas, e a simplificação trófica causada pela perda de predadores de topo, afetam as relações tróficas em três compartimentos conectados da teia alimentar: i) microbiota aquática (algas, ciliados, flagelados e zooplâncton), ii) macroorganismos aquáticos (macroinvertebrados) e iii) múltiplos predadores terrestres de diferentes grupos funcionais, por exemplo, predadores mais ativos (cursoriais) e estacionários (e.g., construtores de teias).  Nós descobrimos que os impactos do aquecimento e da simplificação trófica em cada compartimento aquático (macro e microorganismos) e terrestre da cadeia alimentar dependem do grupo funcional, nível trófico e do componente da comunidade investigado, ou seja, abundância ou riqueza.

Figura 2. (1-4) Bromélias-tanque experimentais em um sub-bosque de Mata Atlântica, bem como os detalhes da vista superior da bromélia, os aquecedores de aquário e sensor de temperatura dentro dos tanques. Créditos da foto: Pablo Antiqueira. (5) Pablo Antiqueira coletando água dos tanques de uma bromélia para avaliar as comunidades da microfauna e algas. Créditos da foto: Gustavo Migliorini. (6) Uma larva de libélula (Leptagrion andromache), um predador de topo que habita o ecossistema de bromélia-tanque, predando uma larva de besouro da família Scirtidae, um grupo de detritívoros comum que habita microecossistemas de bromélia-tanque. Créditos da foto: Pablo Antiqueira.

A simplificação trófica, causada pela perda do predador aquático de topo, impactou substancialmente os três compartimentos da cadeia alimentar. A simplificação trófica aumentou a riqueza e a abundância de organismos filtradores (larvas de mosquitos – Culicidae) no compartimento da macrofauna aquática, direta e indiretamente, por meio de um aumento na riqueza de detritívoros, provavelmente por meio de uma interação facilitadora. Por exemplo, a atividade dos detritívoros gera partículas finas de matéria orgânica, fezes e microrganismos que se alimentam desse material, que, por sua vez são consumidos pelos filtradores. Assim, o aumento de detritívoros aquáticos após a extinção dos predadores de topo também beneficiou os organismos filtradores, aumentando sua riqueza e abundância. Por outro lado, o rebaixamento trófico diminuiu a riqueza de algas no compartimento da microfauna, diminuindo a entrada de nutrientes das atividades biológicas dos predadores (através das fezes e carcaças de presas).

Além disso, o aumento dos filtradores aquáticos devido à perda de predadores de topo aquáticos desencadeou um aumento nos predadores terrestres por meio do efeito cascata nos ecossistemas. Os predadores terrestres mais ativos responderam mais à simplificação trófica aquática, por meio de um aumento na riqueza de espécies da macrofauna, do que os predadores terrestres mais estacionários. O aquecimento não afetou os micro-organismos ou macroorganismos aquáticos, mas aumentou a abundância de predadores terrestres construtores de teias. Nossos resultados fornecem novas evidências sobre como o aquecimento e a simplificação trófica podem afetar a cadeia alimentar de macro e micro-organismos, não apenas no ecossistema aquático, mas também no ecossistema terrestre adjacente por meio de efeitos entre ecossistemas.

Pablo é um ecólogo interessado nos fatores que regulam a estrutura da comunidade e o funcionamento de ecossistemas. A pesquisa de Pablo visa aprofundar a compreensão de como os elementos críticos das mudanças globais alteram a biodiversidade e o funcionamento de ecossistemas. Pablo é pesquisador de pós-doutorado no departamento de Biologia Animal da Universidade Estadual de Campinas (Unicamp), Brasil.  @Pablo Antiqueira

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

Elton Prize Early Career Researcher Shortlist Announced

The Elton Prize is awarded each year for the best paper in the Journal of Animal Ecology written by an early career author at the start of their research career.

The overall winner is selected by the Senior Editors of the journal, and will be announced in the coming weeks. Watch this space! This year’s shortlisted candidates are announced below.

The shortlisted candidates are:

Santiago Agustín Parra, Interaction fidelity is less common than expected in plant-pollinator communities

Dylan Jones, Latitudinal gradient in species diversity provides high niche opportunities for a range-expanding phytophagous insect – Why not check out Dylan’s blog post?

Paulina Arancibia, Network topology and patch connectivity affect dynamics in experimental and model metapopulations – Why not check out Paulina’s blog post about her research.

Ana Payo-Payo, Modelling the responses of partially-migratory metapopulations to changing seasonal migration rates: from theory to data. 

Robert Semmler, Reef fishes weaken dietary preferences after coral mortality, altering resource overlap

Vinícius Caldart, Function of a multimodal signal: a multiple hypothesis test using a robot frog

Pablo Antiqueira Warming and top predator loss drive direct and indirect effects on multiple trophic groups within and across ecosystems

Mélanie Thierry Multiple parasitoid species enhance top-down control, but parasitoid performance is context dependent – why not check out Mélanie’s blog post about her research.

Congratulations to all of our shortlisted candidates! We have received a high volume of excellent applications – those selected above should be extremely proud of their work! Thank you to all authors who submitted an application for the award.

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.

请在此阅读中文版的博文

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

陆生生态系统垂直维度中的生态格局与过程

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.

陆生植被所形成的垂直结构为生物多样性的发生、扩散和繁衍提供了重要的栖息地。从地面到林冠,食物资源,微气候与栖息地结构的变化在较短的空间距离上形成了复杂的环境梯度组合。在这篇综述里,我们探讨总结了垂直维度如何成为森林物种生态进化的重要驱动力,并如何在大的空间和时间尺度上塑造了生物地理格局。

垂直维度中的生态格局

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。

图一.(A)温带森林和(B)热带森林的垂直结构。图片来源:(A)邢爽,(B)常馨月。
垂直维度中的生态机制

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
未来研究方向

我们鼓励生态学家们关注和投入到对于生态系统多维度性的研究中,并围绕垂直维度来验证生态学理论。我们建议唯有在水平维度之上加以对垂直维度中的格局,过程和机制的思考,才能全面的了解物种分布形成的机制以及物种将如何应对全球变化。

关于作者

我是来自中山大学的助理教授邢爽。我研究物种和生态网络对环境变化的响应。我的研究致力于理解物种和生态系统在气候变化,森林丧失和野生动物贸易等综合威胁下的脆弱性。

Twitter账号:@ShannonXing