Can metabolic traits limit species invasions under climate change?

Lead Research Organisation: UNIVERSITY OF EXETER
Department Name: Biosciences

Abstract

Invasive species are currently considered second only to habitat loss as a cause of rapid and undesirable changes in the functioning of ecosystems worldwide. In the United Kingdom alone, the annual cost of invasive species is estimated to be ~£1.7 billion. In this context, major cause for concern is that human-mediated species translocations and global warming are both causing rapid shifts in species' ranges and phonologies at an escalating rate. For example, a Pacific diatom Neodenticula seminae was documented into the North Atlantic for the first time in 800,000 years due to climate-driven melting of the Arctic ice cap and changes in ocean circulation. Such abrupt introductions can result in novel interactions (e.g., predator-prey or resource competition), which then have the potential to result in disruptive invasions of non-native species into local communities.

In this project, we will meet the challenge of developing a general framework for predicting invasion success by building the first-ever global database on the temperature dependence of metabolic (physiological) traits relevant to species invasions through interactions, use these data to develop and parameterize a novel theoretical framework, and test some key predictions of this theory using laboratory experiments with a globally important functional group, the Phytoplankton (photosynthetic unicellular marine and freshwater algae and bacteria). Phytoplankton form the base of form the base of most aquatic food webs and contribute over half of global primary production.

We will address three core questions:

(1) How will mismatches in how metabolic traits (e.g., respiration and photosynthesis rate) of natives and non-native species respond to temperature change affect invasions?
This question is important because new species often arrive with the physiological "baggage" of the environment they originated in, and therefore may be poorly adapted to their new environment (at least initially).

(2) Does the rate and magnitude of thermal acclimation (defined as phenotypic changes in thermal-response with change in environmental temperature) in a non-native species to its new environment influence its invasion success?
This question is important because many species can overcome the initial disadvantage of a novel environment by rapidly adjusting the way their metabolism responds to temperature.

(3) Are natural temperature cycles important determinants of invasion success?
This question is important because species invasions, especially in temperate regions, take place in climates that change cyclically at daily (say-night cycles) and seasonal (e.g., winter-summer) scales. Therefore, a non-native species that arrives, say, in winter, may have a lesser chance of invading successfully than if it arrived in summer.

Overall, this study will fill a major gap in our understanding of the importance of metabolic constraints on species interactions for species invasions. We expect our results to form a new and robust foundation for predicting species invasions in natural as well as human-dominated environments. Our global database on metabolic traits will be a valuable, long-term resource for mapping metabolic traits onto potentially invasive species, and also for parameterizing ongoing efforts to model the effects of climate change on ecosystem services, including the carbon cycle.

Planned Impact

By establishing Project Partnerships with CR and IA, we plan to develop synergistic links between this project and the Sir Alister Hardy Foundation for Ocean Science (SAHFOS) and Plymouth Marine Laboratories (PML) (through IA) respectively, towards achieving their goals. Other beneficiaries may include middle-user (applied research) organizations and end-user (direct application) organizations involved in invasive species management, native species conservation, and modeling effects of climate change on ecosystem services, including the International Union for the Conservation of Nature (IUCN) Invasive Species Specialist Group (ISSG), Centre for Environment, Fisheries and Aquaculture Science (Cefas), UK Met Office, Institute of Zoology (IOZ), and the end-user bodies they advise. SAHFOS and PML support the research as Project Partners, contributing time, expertise, and data. This commitment indicates their expectation that the research will help fulfill their goals.

How SAHFOS will benefit: A major part of SAHFOS research seeks to understand and predict the role of climate in multi-trophic marine range and regime shifts (potentially through species translocations, and resulting invasions) being documented by their Continuous Plankton Recorder. Therefore, the outputs of our research components (global database, theoretical framework, phytoplankton experiments) are of strong interest to SAHFOS, and potentially, their clients, which include the EU, WWF, World Bank, UK and government departments such as the Department for Environment, Food, and Rural Affairs (DEFRA), and the International Council for the Exploration of the Sea. Specifically, our empirically grounded invasion framework will enable the development of new and better range and regime shift models under climate change.

How PML will benefit: PML is an International Centre of Excellence in Marine Science & Technology and a Collaborative Centre of NERC that carries out innovative and timely fundamental, strategic and applied research in the marine environment from the uppermost reaches of estuaries to the open ocean. It is an independent, impartial provider of scientific research in the marine environment with a focus on understanding biodiversity and ecosystem function, biogeochemical cycling, pollution and health, and forecasting the role of the oceans in the Earth System with an outstanding reputation at a national and international level. Our research outputs will play a key role in PML's European Regional Seas Ecosystem Model (ERSEM) modelling initiative, which seeks to enhance our capacity to assess the physical, chemical and biological controls on biogeochemical cycling, with a focus on the NW European Shelf. This initiative is a component of the NERC-Defra Shelf Seas Biogeochemistry program, PML, Cefas and NOC in collaboration with the UKMO. Specifically, our metabolic trait based framework will help introduce species invasion dynamics in to the ERSEM model, and our database will aid in improving the description of size / functional class diversity, and within trait diversity of thermal responses, which can have far-reaching ecosystem impacts. It will also help ERSEM achieve one of its core goals - to expand the thermally dependent trait diversity of autotrophs, zooplankton and zoobenthos towards understanding how these groups drive energy supply into the ecosystem and its transfer to higher trophic levels.

PDRA Training: The three PDRAs will receive specialized and technically advanced training in computing, statistics, mathematical modeling and physiological and population dynamics experimentataion. These are all highly marketable skills in many sectors. PDRA job prospects outside academia will benefit from their association with PML and SAHFOS.

Publications

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Description 1. In september of last year (2015) we finished an experiment in metabolic thermal adaptation in the green alga, Chlorella vulgaris. This was the fist piece of work to demonstrate how the evolution of traits that influence metabolic performance can explain the how tolerance to warming evolves in the autotrophs. This work was published last year in Ecology Letters.

2. We have just begun the 2nd large experiment in the grant, which focuses on 6 species and will characterise the temperature dependence of the functional response for nutrient uptake. We will then use this information to build and paramterise models of interspecific competition.

3. Over the last year we completed an experiment with Chlamydomonas reinhardtii, which we isolated from our long-term warming experiment in Dorset. We characterised the thermal physiology and competitive abilities of the warm- and ambient-adapted isolates. This work is now in-press in Nature Ecology and Evolution and is the first work to identify the mechanisms of thermal adaptation in phytoplankton outside of the laboratory.

4. We have now finished the large 6 species experiment described above (point 2) and are in the process of analysing the data and testing the theory developed by our collaborators at Imperial college. We envision writing this work up over the next 6 months.

5. In the last year we have written up the results of the main experiment. This manuscript is now published in Ecology Letters and demonstrates that were able to predict the outcome of competition in 72% of pairwise experiments using our new model based on metabolic thermal traits.
Exploitation Route Our paper on the evolution of elevated thermal tolerance and phytoplankton competition provide the basis for incorporating more detailed ecological and evolutionary dynamics into models of aquatic productivity.
Sectors Environment

 
Title Data and code from: Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints 
Description To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness-related rates to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can-at least partly-overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta-analysis of the thermal performance curves of growth rate of phytoplankton-a globally important functional group-, controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak "hotter-is-better" constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.63xsj3tzv