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

Sidnie Manton Award: submit your proposal now

Early career ecologist? If you have an idea for a Review or Long-term Studies in Animal Ecology paper, we invite you to submit a short abstract and be in with a chance of winning our next Sidnie Manton Award.

Proposals will be assessed by the journal Editors and successful applicants will be invited to submit a manuscript to Journal of Animal Ecology. Submitted manuscripts will then go through our usual peer review process and, of those published, an overall winner will be selected.

The British Ecological Society and Journal of Animal Ecology have long-championed the research of early career* ecologists and, through the Sidnie Manton Award, we aim to continue this tradition. Meet the most recent winners of the award, Diego Ellis Soto and Kristy M. Ferraro, here. Following on from their winning paper, Diego and Kristy also collated the Virtual Issue, Animal-vectored subsidies.

If you’d like some tips for writing Reviews or Long-term Studies, don’t miss our free-to-read Editorial, Time counts in Animal Ecology.

Submit your proposal for the Sidnie Manton Award here.

Deadline: 17 February 2023

The winning paper will feature prominently in the journal and the recipient of the award will receive £250, a 12-month membership of the British Ecological Society (BES) and free registration for the BES Annual Meeting if they choose to attend to present their current research.

*Early career is defined as less than five years post- Ph.D. or -D.Phil. experience according to the date of your graduation certificate. Reasonable exceptions will be considered (e.g. for parental leave or a substantial shift in research area).

Winners announced: Sidnie Manton Award 2022

Celebrating the best Review or Long-term Studies in Animal Ecology paper by an early career researcher, the Journal of Animal Ecology Editors are pleased to announce the winners of the third (2022) Sidnie Manton Award as Diego Ellis Soto and Kristy M. Ferraro.
Diego and Kristy’s winning paper, A methodological roadmap to quantify animal-vectored spatial ecosystem subsidies addresses the important realisation that animals can exert strong influences on ecosystems, and connect them, via the deposition of subsidies.

Couched in meta-ecosystem theory, the paper outlines a roadmap illustrating how future empirical studies could integrate data from spatial trophic structure, habitat structure, resource selection, and animal and resource movement. Importantly, it also highlights two case studies that illustrate the power of the approach.

The Journal of Animal Ecology Editors see the work of these early career ecologists and their colleagues as an important guide for future research on how animals influence the structure and dynamics of ecosystems. 

Get to know the winners and the story behind their research in our Q&A below.

If you’re an early career researcher with an idea for a Review or Long-term Studies in Animal Ecology paper, submit a proposal now. You could be in line for the next Sidnie Manton Award!
Winner Q&A: Diego Ellis Soto and Kristy M. Ferraro

Congratulations on your award! Can you share a bit of background about yourselves and how you got into ecology?

Diego:  Coming from an itinerant family, I have been fortunate to experience and relish a variety of cultures and landscapes. As an aspiring undergraduate in environmental sciences, I had the opportunity to travel to the Galápagos. Exploring the volcanic landscape that harbors lethargic giant tortoises, flightless cormorants and Darwin finches became a life-changing experience that fueled my desire and passion to become an ecologist and naturalist. I have always been on the move, which led to my passion for travel and desire to learn how animals do it across the world – otherwise known as movement ecology – and how they affect and interact with ecosystems.

Kristy: I’ve always been interested in the ways animals matter; from their roles in ecosystems to how humans think about and interact with them. This passion led me to ecology, and specifically to zoogeochemistry. Now I get to study fascinating animals and explore the intricate relationship they have with the world around them. I also believe that, as we learn more about ecosystems and animals, we begin to appreciate their complexity. And when we view something as complex, we’re more likely to treat it with respect.

What can you tell us about your winning Review article, A methodological roadmap to quantify animal-vectored spatial ecosystem subsidies?

Animals are always on the move and, through what they eat, where they die, and where they urinate and defecate, they move nutrients with them. Only recently has the role of larger animals in nutrient cycles been recognised as significant. This is especially relevant under climate change, as rewilding certain areas with animals could be a nature-based solution to offset carbon emissions.

The challenge is understanding where, when, and how much, animals distribute nutrients across ecosystem. It relies on methods and concepts from a variety of scientific disciplines and there is a lot to consider.

To help guide ecologists, we developed a roadmap, demonstrating how to integrate the necessary disciplines of animal ecology, ecosystem ecology, remote sensing, and biogeochemistry, to conduct robust research to understand, quantify, and estimate animal contributions to nutrient cycles.

What did you enjoy most about conducting this research?

This paper was a great opportunity for us to dive into how to best quantify the ways in which animals move nutrients across ecosystems, also known as zoogeochemical research. As early career scientists, we are trying to take a critical and intentional approach to the study of animal-ecosystem interactions. Here we’ve made a roadmap for ourselves and others, paving the way for an integrative approach to this type of work.

This project also gave us the opportunity to work with a diverse team. Bridging together desperate fields, including ecosystem ecology, animal ecology, biogeochemistry, and remote sensing was extremely rewarding, and allowed us all to learn from each other. Despite tackling zoogeochemical research in a slightly different ways and across locations and species, it was fascinating to find certain commonalities in some of the tools we used, and limitations of others.

Have you continued this research and if so, where are you at now with it?

We have both begun implementing the roadmap ­­­­– on completely different ecosystems, contexts and species!

Diego: I am exploring the effects that Galapagos giant tortoises have on ecosystems. This ranges from understanding how giant tortoises migrate up and down volcanoes, to linking this voyage with the seed dispersal of endemic and introduced species into the Galápagos National Park; up to understanding how they may connect terrestrial and aquatic ecosystems. I believe that giant tortoises can be seen as a combination of hippos and elephants in the Galápagos due to the ecosystem services they provide. After my PhD, I am interested in linking ecosystem services provided by animals to an entire community of species in a regional study site.

Kristy: I am working on several projects that look at how northern ungulates (caribou, elk, white-tailed deer, and mule deer) are impacting ecosystem nutrient distribution, nitrogen cycling, and carbon storage. By combining field experiments with GPS data informed agent based models, I aim to first quantify the ways in which these mammals are impacting nutrient cycling and then model how these impacts are distributed at the landscape scale. This integrative approach directly applies the roadmap we propose in our paper, and sheds light on the way animals are moving vital nutrients around their home range.    

Read the winning paper, A methodological roadmap to quantify animal-vectored spatial ecosystem subsidies

Early career researchers: apply for the next Sidnie Manton Award
To be considered for the next Sidnie Manton Award, submit your proposal for a Review or a Long-term Studies in Animal Ecology paper by 17 February 2023.
Applications will be assessed by the journal Editors and successful applicants will be invited to submit a manuscript to Journal of Animal Ecology. Submitted manuscripts will then go through our usual peer review process and, of those published, an overall winner will be selected.

Shortlist Announced for Elton Prize Early Career Researcher Award

Each year Journal of Animal Ecology awards the Elton Prize to the best Research Article in the journal by an early career researcher. Today we present the shortlisted papers for this year’s award, based on the 2021 (90th) volume of the journal.
The winner will be selected in the coming weeks so follow the blog and watch this space for future announcements!
This year’s shortlisted candidates are:

Cristina Botías, Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies

Ellen Brandell, Group density, disease, and season shape territory size and overlap of social carnivores

Joseph Burant, Early warning indicators of population collapse in a seasonal environment

Félicie Dhellemmes, Personality-driven life history trade-offs differ in two subpopulations of free-ranging predators

Phoebe Edwards, A mechanism for population self-regulation: Social density suppresses GnRH expression and reduces reproductivity in voles

Emily Le Sage, Preparatory immunity: Seasonality of mucosal skin defences and Batrachochytrium infections in Southern leopard frogs

Tamika Lunn, Spatial dynamics of pathogen transmission in communally roosting species: Impacts of changing habitats on bat-virus dynamics

Kate Pereira Maia, Interaction generalisation and demographic feedbacks drive the resilience of plant–insect networks to extinctions

Allison M. Roth, Sexual selection and personality: Individual and group-level effects on mating behaviour in red junglefowl

Sidnie Manton Award for early career ecologists – Submit your proposals now!

87_i3_CoverWe are excited to announce that the Sidnie Manton Award is open for proposals.  With this award, we aim to inspire early career researchers working on any aspect of animal ecology to publish review or synthesis papers that might either summarize their dissertation work, provide new insights into classic areas of animal ecology, or shed light on emerging fields.

The British Ecological Society and Journal of Animal Ecology have championed the research of early career ecologists for a very long time and though the Sidnie Manton Award we aim to continue this tradition. This is the second time the journal has run the competition and presented the Sidnie Manton Award, more about Sidnie Manton and the 2018 winner, Ben Weinstein, is available in this Editorial.

To enter, please submit an abstract of your proposed Review or a Synthesis paper here. DEADLINE EXTENDED TO by Sunday 7 October 2018.

Proposed papers should fit the Aims and Scope of the Journal and be a timely and novel contribution to the study of animal ecology.

Applicants should have commenced their PhD no more than 7 years prior to the deadline, although reasonable exceptions will be considered (e.g. career breaks, part-time study or substantial shift in research area).

The award will be presented to the early career researcher who proposed the article and who should take responsibility for leading and writing the paper.

The Senior Editors will evaluate the proposals and invite authors of papers showing exceptional promise to submit their paper by January 2019. All papers that successfully pass the review process will be published.

The winning paper will feature prominently in the Journal and the recipient of the award will receive £250, a 12-month membership of the British Ecological Society (BES) and free registration for the BES annual meeting if they choose to attend to present their current research.

Enter Now