Eutrophication governs predator-prey interactions and temperature effects in  Aedes aegypti  populations

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Abstract

Background

Mosquito population dynamics are driven by large-scale (e.g. climatological) and small-scale (e.g. ecological) factors. While these factors are known to independently influence mosquito populations, it remains uncertain how drivers that simultaneously operate under natural conditions interact to influence mosquito populations. We, therefore, developed a well-controlled outdoor experiment to assess the interactive effects of two ecological drivers, predation and nutrient availability, on mosquito life history traits under multiple temperature regimes.

Methods

We conducted a temperature-controlled mesocosm experiment in Kruger National Park, South Africa, with the yellow fever mosquito, Aedes aegypti. We investigated how larval survival, emergence and development rates were impacted by the presence of a locally-common invertebrate predator (backswimmers Anisops varia Fieber (Notonectidae: Hemiptera), nutrient availability (oligotrophic vs eutrophic, reflecting field conditions), water temperature, and interactions between each driver.

Results

We observed that the effects of predation and temperature both depended on eutrophication. Predation caused lower adult emergence in oligotrophic conditions but higher emergence under eutrophic conditions. Higher temperatures caused faster larval development rates in eutrophic but not oligotrophic conditions.

Conclusions

Our study shows that ecological bottom-up and top-down drivers strongly and interactively govern mosquito life history traits for Ae. aegypti populations. Specifically, we show that eutrophication can inversely affect predator–prey interactions and mediate the effect of temperature on mosquito survival and development rates. Hence, our results suggest that nutrient pollution can overrule biological constraints on natural mosquito populations and highlights the importance of studying multiple factors.

Electronic supplementary material

The online version of this article (10.1186/s13071-019-3431-x) contains supplementary material, which is available to authorized users.

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Most cited references 40

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Interactions among ecosystem stressors and their importance in conservation.

Isabelle M. Côté, Emily S Darling, Christopher J Brown (2016)

Interactions between multiple ecosystem stressors are expected to jeopardize biological processes, functions and biodiversity. The scientific community has declared stressor interactions-notably synergies-a key issue for conservation and management. Here, we review ecological literature over the past four decades to evaluate trends in the reporting of ecological interactions (synergies, antagonisms and additive effects) and highlight the implications and importance to conservation. Despite increasing popularity, and ever-finer terminologies, we find that synergies are (still) not the most prevalent type of interaction, and that conservation practitioners need to appreciate and manage for all interaction outcomes, including antagonistic and additive effects. However, it will not be possible to identify the effect of every interaction on every organism's physiology and every ecosystem function because the number of stressors, and their potential interactions, are growing rapidly. Predicting the type of interactions may be possible in the near-future, using meta-analyses, conservation-oriented experiments and adaptive monitoring. Pending a general framework for predicting interactions, conservation management should enact interventions that are robust to uncertainty in interaction type and that continue to bolster biological resilience in a stressful world.

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Net effects of multiple stressors in freshwater ecosystems: a meta-analysis

Michelle Jackson, Charlie J. G. Loewen, Rolf Vinebrooke … (2016)

The accelerating rate of global change has focused attention on the cumulative impacts of novel and extreme environmental changes (i.e. stressors), especially in marine ecosystems. As integrators of local catchment and regional processes, freshwater ecosystems are also ranked highly sensitive to the net effects of multiple stressors, yet there has not been a large-scale quantitative synthesis. We analysed data from 88 papers including 286 responses of freshwater ecosystems to paired stressors and discovered that overall, their cumulative mean effect size was less than the sum of their single effects (i.e. an antagonistic interaction). Net effects of dual stressors on diversity and functional performance response metrics were additive and antagonistic, respectively. Across individual studies, a simple vote-counting method revealed that the net effects of stressor pairs were frequently more antagonistic (41%) than synergistic (28%), additive (16%) or reversed (15%). Here, we define a reversal as occurring when the net impact of two stressors is in the opposite direction (negative or positive) from that of the sum of their single effects. While warming paired with nutrification resulted in additive net effects, the overall mean net effect of warming combined with a second stressor was antagonistic. Most importantly, the mean net effects across all stressor pairs and response metrics were consistently antagonistic or additive, contrasting the greater prevalence of reported synergies in marine systems. Here, a possible explanation for more antagonistic responses by freshwater biota to stressors is that the inherent greater environmental variability of smaller aquatic ecosystems fosters greater potential for acclimation and co-adaptation to multiple stressors.

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The ecology of climate change and infectious diseases

Kevin Lafferty (2009)

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Author and article information

Contributors

Louie Krol: l.krol@umail.leidenuniv.nl

Erin E. Gorsich: erin.gorsich@warwick.ac.uk

Ellard R. Hunting: e.r.hunting@bristol.ac.uk

Danny Govender: danny.govender@sanparks.org

Peter M. van Bodegom: p.m.van.bodegom@cml.leidenuniv.nl

Maarten Schrama:

ORCID: http://orcid.org/0000-0001-9803-6244

m.j.j.schrama@cml.leidenuniv.nl

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 24 April 2019

Publication date PMC-release: 24 April 2019

Publication date Collection: 2019

Volume: 12

Electronic Location Identifier: 179

Affiliations

[1 ]ISNI 0000 0001 2312 1970, GRID grid.5132.5, Institute of Environmental Sciences, , Leiden University, ; Leiden, The Netherlands

[2 ]ISNI 0000 0001 2159 802X, GRID grid.425948.6, Naturalis Biodiversity Centre, ; Leiden, The Netherlands

[3 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, The Zeeman Institute for Systems Biology & Infectious Disease Epidemiology Research, , University of Warwick, ; Coventry, UK

[4 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, School of Life Sciences, , University of Warwick, ; Coventry, UK

[5 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Biological Sciences, , University of Bristol, ; Bristol, UK

[6 ]ISNI 0000 0004 0504 7510, GRID grid.56466.37, Department of Biology, , Woods Hole Oceanographic Institution, ; Woods Hole, MA USA

[7 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Department of Paraclinical Sciences, , University of Pretoria, ; Pretoria, South Africa

[8 ]GRID grid.452838.0, Scientific Services Kruger National Park, ; Skukuza, South Africa

Author information

Maarten Schrama http://orcid.org/0000-0001-9803-6244

Article

Publisher ID: 3431

DOI: 10.1186/s13071-019-3431-x

PMC ID: 6480876

PubMed ID: 31014388

SO-VID: 646b0500-5c19-4e87-898a-f74e90961748

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 10 October 2018

Date accepted : 4 April 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100007442, Gratama Stichting;

Award ID: 2016.08

Award Recipient : Maarten Schrama

Funded by: FundRef http://dx.doi.org/10.13039/100006734, Princeton University;

Award ID: RCN-IDEAS

Award Recipient : Erin E. Gorsich

Funded by: FundRef http://dx.doi.org/10.13039/501100010195, Uyttenboogaart-Eliasen Stichting;

Award ID: SUB.2016.12.08

Award Recipient : Maarten Schrama

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: ecological drivers,vector-borne,anthropogenic pressures,interaction effects,temperature,biodiversity decline

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: ecological drivers, vector-borne, anthropogenic pressures, interaction effects, temperature, biodiversity decline

Eutrophication governs predator-prey interactions and temperature effects in Aedes aegypti populations

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Abstract

Background

Methods

Results

Conclusions

Electronic supplementary material

Related collections

Vector Biology

Most cited references 40

Interactions among ecosystem stressors and their importance in conservation.

Net effects of multiple stressors in freshwater ecosystems: a meta-analysis

The ecology of climate change and infectious diseases

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Contributors

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Affiliations

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