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Stoichiometric mismatch causes a warming-induced regime shift in experimental plankton communities
Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och geovetenskap. Department Biologie II, Ludwig-Maximilians-Universität München,Planegg, Germany.ORCID-id: 0000-0002-3860-5051
Department Biologie II, Ludwig-Maximilians-Universität München,Planegg, Germany; Department of Experimental Limnology,Leibniz Institute of Freshwater Ecologyand Inland Fisheries (IGB), Stechlin,Germany.
Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och geovetenskap. Department of Experimental Limnology,Leibniz Institute of Freshwater Ecologyand Inland Fisheries (IGB), Stechlin,Germany.
Department Biologie II, Ludwig-Maximilians-Universität München,Planegg, Germany.
2022 (Engelska)Ingår i: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, artikel-id e3674Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

In many ecosystems, consumers respond to warming differently than their resources, sometimes leading to temporal mismatches between seasonal maxima in consumer demand and resource availability. A potentially equally pervasive, but less acknowledged threat to the temporal coherence of consumer-resource interactions is mismatch in food quality. Many plant and algal communities respond to warming with shifts toward more carbon-rich species and growth forms, thereby diluting essential elements in their biomass and intensifying the stoichiometric mismatch with herbivore nutrient requirements. Here we report on a mesocosm experiment on the spring succession of an assembled plankton community in which we manipulated temperature (ambient vs. +3.6°C) and presence versus absence of two types of grazers (ciliates and Daphnia), and where warming caused a dramatic regime shift that coincided with extreme stoichiometric mismatch. At ambient temperatures, a typical spring succession developed, where a moderate bloom of nutritionally adequate phytoplankton was grazed down to a clear-water phase by a developing Daphnia population. While warming accelerated initial Daphnia population growth, it speeded up algal growth rates even more, triggering a massive phytoplankton bloom of poor food quality. Consistent with the predictions of a stoichiometric producer–grazer model, accelerated phytoplankton growth promoted the emergence of an alternative system attractor, where the extremely low phosphorus content of the abundant algal food eventually drove Daphnia to extinction. Where present, ciliates slowed down the phytoplankton bloom and the deterioration of its nutritional value, but this only delayed the regime shift. Eventually, phytoplankton also grew out of grazer control in the presence of ciliates, and the Daphnia population crashed. To our knowledge, the experiment is the first empirical demonstration of the “paradox of energy enrichment” (grazer starvation in an abundance of energy-rich but nutritionally imbalanced food) in a multispecies phytoplankton community. More generally, our results support the notion that warming can exacerbate the stoichiometric mismatch at the plant–herbivore interface and limit energy transfer to higher trophic levels.

Ort, förlag, år, upplaga, sidor
Ecological Society of America , 2022. artikel-id e3674
Nyckelord [en]
alternative states, C:P ratio, Daphnia, ecological stoichiometry, food quality, mesocosm experiment, paradox of energy enrichment, plant-herbivore, temperature, warming
Nationell ämneskategori
Ekologi
Identifikatorer
URN: urn:nbn:se:umu:diva-124874DOI: 10.1002/ecy.3674ISI: 000780007500001Scopus ID: 2-s2.0-85127759512OAI: oai:DiVA.org:umu-124874DiVA, id: diva2:956160
Forskningsfinansiär
Knut och Alice Wallenbergs Stiftelse, 016.0083Vetenskapsrådet, 621-2010-5316
Anmärkning

Originally included in thesis in manuscript form.

Tillgänglig från: 2016-08-29 Skapad: 2016-08-29 Senast uppdaterad: 2024-07-02Bibliografiskt granskad
Ingår i avhandling
1. Effects of warming and nutrient enrichment on feeding behavior, population stability and persistence of consumers and their resources
Öppna denna publikation i ny flik eller fönster >>Effects of warming and nutrient enrichment on feeding behavior, population stability and persistence of consumers and their resources
2016 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
Abstract [en]

Consumer-resource interactions are the basic building blocks of every food web. In spite of being a central research theme of longstanding interest in ecology, the mechanisms governing the stability and persistence of consumer-resource interactions are still not entirely understood. In particular, theoretical predictions on consumer-resource stability along gradients of temperature and nutrient enrichment diverge widely and are sometimes in conflict with empirical results. In this thesis I address these issues from the angle of the functional response, which describes a consumer’s feeding rate as a function of resource density. Specifically, I explore mechanistic, nutrient-based consumer-resource interaction models with respect to the influence of feeding behavior (the shape of the functional response), environmental temperature, nutrient enrichment, and resource quality on consumer-resource stability and persistence. In order to parameterize these models I performed extensive laboratory experiments with pairs of freshwater pelagic algae and grazers of the genus Daphnia, which are widespread, ecologically important model organisms.

I found a sigmoidal type III functional response in every studied Daphnia-algae species pair. The exact form of its shape is described by an exponent b which is determined by fitting functional response models to the experimental data. A high value of b can stabilize consumer-resource systems under the otherwise destabilizing influence of nutrient enrichment, as predicted by a novel stability criterion relating b to the consumer’s prey handling time, food conversion efficiency and mortality. Estimated parameter values and, consequently, stability predictions are sensitive to the method of parameter estimation, and I propose a new estimation procedure that minimizes parameter uncertainty. Because many consumers’ feeding rates depend on temperature, warming is expected to strongly affect food web stability. In functional response experiments over a broad temperature gradient, I found that the attack rate coefficient and the maximum ingestion rate of Daphnia are hump-shaped functions of temperature. Moreover, the functional response exponent increases with warming towards stronger type III responses. Plugging these findings into a nutrient-based consumer-resource model, I found that predator persistence is a U-shaped function of temperature in nutrient enrichment-temperature space. Enrichment easily turns the system unstable when the consumer has a type II response, whereas a type III response opens up a large region of stability at intermediate, for the consumer optimal, temperatures. These findings reconcile seemingly conflicting results of earlier studies of temperature effects on consumer-resource dynamics, which can be mapped as special cases onto the enrichment-temperature space. I finally demonstrate the utility of three key model ingredients - temperature dependence of rate parameters, a mechanistic description of the dynamics of algal resources, and a type III functional response in Daphnia - by successfully implementing them in the description and explanation of phytoplankton-Daphnia dynamics in a mesocosm experiment exploring effects of warming on the spring succession of the plankton.

Ort, förlag, år, upplaga, sidor
Umeå: Umeå University, 2016. s. 27
Nyckelord
consumer-resource, Daphnia, functional response, nutrient enrichment, parameter estimation, persistence, plankton, predator-prey, stability, temperature, type II, type III, warming
Nationell ämneskategori
Ekologi
Identifikatorer
urn:nbn:se:umu:diva-124876 (URN)978-91-7601-544-5 (ISBN)
Externt samarbete:
Disputation
2016-09-20, Lilla Hörsalen (KB3A9), KBC, Umeå University, Umeå, 09:30 (Engelska)
Opponent
Handledare
Tillgänglig från: 2016-08-30 Skapad: 2016-08-29 Senast uppdaterad: 2024-07-02Bibliografiskt granskad

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