Can metabolic traits limit species invasions under climate change?

Lead Research Organisation: Imperial College London
Department Name: Life Sciences

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.
 
Description We have completed progress with all three---ecoinformatics, modelling and experiments components---of the grant.

On the ecoinformatics front, we built a new global metabolic traits database, BioTraits, which has now grown to 60,029 temperature response measurements from 1083 species. We have published nine papers, and have submitted three more based on this database.

On the modelling front, we developed models for competition and invasion between pairs of phytoplankton, and have been successful in fitting the models to experimental data. Two papers based on this work have been accepted.

We also developed a mathematical model that captures the contributions of photosynthesis, respiration and uptake/allocation efficiency in autotrophs to population growth and consequently, invasions and competition between species leading to a paper.
Exploitation Route By using the global Biotraits database for meta-analyses and calibrate parameterizations of ecosystem and global change models. The theory we have developed can be extended to more complex, multi-trophic systems.
Sectors Agriculture, Food and Drink,Environment

 
Description We have developed a invasion/assembly video game using the findings from our research - please see ecobuildergame.org We are using it to teach school children as well as the general public about species invasions and community assembly.
First Year Of Impact 2016
Sector Education
Impact Types Societal

 
Description A Novel Framework for Predicting Emerging Chemical Stressor Impacts in Complex Ecosystems
Amount £622,707 (GBP)
Funding ID NE/S000291/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2018 
End 03/2023
 
Description Impacts of global warming in sentinel systems: from genes to ecosystems
Amount £1,815,577 (GBP)
Funding ID NE/M020843/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2015 
End 09/2019
 
Title New Software Package for fitting thermal performance curves in R 
Description A new pipeline to fit thermal performance curves in R applied to Ecology, Evolution and Climate Change Science 
Type Of Material Improvements to research infrastructure 
Year Produced 2021 
Provided To Others? Yes  
Impact New open source software available to researchers worldwide 
URL https://github.com/padpadpadpad/rTPC
 
Title New package for visualizing networks (including food webs) 
Description New Python package: https://github.com/jxz12/s_gd2 
Type Of Material Improvements to research infrastructure 
Year Produced 2018 
Provided To Others? Yes  
Impact New papers arising from the use of this package 
URL https://github.com/jxz12/s_gd2
 
Title BioTraits2 - A global database for Metabolic Traits 
Description Biotraits is a global database of metabolic traits relevant to species invasions through interactions.The new database replaces the original global Biotraits database (Anthony I. Dell, Samraat Pawar, and Van M. Savage 2013. The thermal dependence of biological traits. Ecology 94:1205-1206. http://dx.doi.org/10.1890/12-2060.1). 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? No  
Impact The latest version of this database will go public in July 2019. It will be a primary, long-term resource for institutions and individuals seeking to perform meta-analyses, and parameterize and calibrate ecosystem and global change models. 
 
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
 
Title Data from: Higher temperatures amplify the negative effects of mutations on protein stability 
Description CONTENTS OF THIS DATASET
1) ADK_tree.phy: The ADK gene tree reconstructed for this study.

2) calibrated_species_tree.phy: The relative time-calibrated phylogeny reconstructed for this study.

3) ddG_vs_Temp_interspecific.csv: Weighted median ??G estimates and temperature values for each of the 70 prokaryotic ADKs.

4) ddG_vs_Temp_intraspecific.csv: Median ??G estimates and temperature values for the 6 selected prokaryotic ADKs.
5) ln_K_t_gen_vs_Temp_and_Cell_Volume.csv: Generation time-corrected substitution rate estimates (using a natural logarithm transformation), minimum/maximum cell volume estimates, and temperature values. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_from_Higher_temperatures_worsen_the_effects_of_mutations_...
 
Title Data from: Higher temperatures amplify the negative effects of mutations on protein stability 
Description CONTENTS OF THIS DATASET
1) ADK_tree.phy: The ADK gene tree reconstructed for this study.

2) calibrated_species_tree.phy: The relative time-calibrated phylogeny reconstructed for this study.

3) ddG_vs_Temp_interspecific.csv: Weighted median ??G estimates and temperature values for each of the 70 prokaryotic ADKs.

4) ddG_vs_Temp_intraspecific.csv: Median ??G estimates and temperature values for the 6 selected prokaryotic ADKs.
5) ln_K_t_gen_vs_Temp_and_Cell_Volume.csv: Generation time-corrected substitution rate estimates (using a natural logarithm transformation), minimum/maximum cell volume estimates, and temperature values. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_from_Higher_temperatures_worsen_the_effects_of_mutations_...
 
Title Package for fitting Thermal Response Data to Models 
Description The Grant has lead to the development of a new R Package for fitting thermal response data to mathematical models, called rTPC. 
Type Of Technology Software 
Year Produced 2019 
Open Source License? Yes  
Impact The Methods paper that we published in 2021 has already been cited 39 times. 
URL https://github.com/padpadpadpad/rTPC
 
Description Public exhibition of EcoBuilder game 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact We demonstrated the ecobuilder (ecobuildergame.org) game, which teaches principles of metabolically driven invasions and assembly into complex communities through a video ganme, at two public exhibitions in the greater London area. Our exhibition allowed individuals to play the game - we estimated a total visitation of approx 600 individuals across from school children to adults.
Year(s) Of Engagement Activity 2016
URL http://ecobuildergame.org
 
Description Public exhibition of EcoBuilder game for species invasions 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact We demonstrated the ecobuilder (ecobuildergame.org) game, which teaches principles of metabolically driven invasions and assembly into complex communities through a video ganme, at two public exhibitions in the greater London area (Imperial festival and Silwood Bugs Day). Our exhibition allowed individuals to play the game - we estimated a total visitation of approx 8000 individuals across from school children to adults.
Year(s) Of Engagement Activity 2017
URL http://ecobuildergame.org