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Uszko, Wojciech
Publications (10 of 12) Show all publications
Kalinkat, G., Rall, B. C., Uiterwaal, S. F. & Uszko, W. (2023). Empirical evidence of type III functional responses and why it remains rare. Frontiers in Ecology and Evolution, 11, Article ID 1033818.
Open this publication in new window or tab >>Empirical evidence of type III functional responses and why it remains rare
2023 (English)In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 11, article id 1033818Article in journal (Refereed) Published
Abstract [en]

More than 70 years after its introduction, the framework of resource density-dependent consumption rates, also known as predator-prey functional responses, remains a core concept in population and food web ecology. Initially, three types of responses were defined: linear (type I), hyperbolic (type II), and sigmoid (type III). Due to its potential to stabilize consumer-resource population dynamics, the sigmoid type III functional response immediately became a “holy grail” in population ecology. However, experimentally proving that type III functional responses exist, whether in controlled laboratory systems or in nature, was challenging. While theoretical and practical advances make identifying type III responses easier today, decades of research have brought only a limited number of studies that provide empirical evidence for type III response curves. Here, we review this evidence from laboratory- and field-based studies published during the last two decades. We found 107 studies that reported type III responses, but these studies ranged across various taxa, interaction types, and ecosystems. To put these studies into context, we also discuss the various biological mechanisms that may lead to the emergence of type III responses. We summarize how three different and mutually independent intricacies bedevil the empirical documentation of type III responses: (1) challenges in statistical modeling of functional responses, (2) inadequate resource density ranges and spacing, and (3) biologically meaningful and realistic design of experimental arenas. Finally, we provide guidelines on how the field should move forward based on these considerations.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2023
Keywords
biodiversity, chaos, filter feeder, food webs, population dynamics, predator-prey interactions, resource density, stability
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-206341 (URN)10.3389/fevo.2023.1033818 (DOI)000951811900001 ()2-s2.0-85150701097 (Scopus ID)
Available from: 2023-04-28 Created: 2023-04-28 Last updated: 2023-04-28Bibliographically approved
Diehl, S., Berger, S., Uszko, W. & Stibor, H. (2022). Stoichiometric mismatch causes a warming-induced regime shift in experimental plankton communities. Ecology, Article ID e3674.
Open this publication in new window or tab >>Stoichiometric mismatch causes a warming-induced regime shift in experimental plankton communities
2022 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, article id e3674Article in journal (Refereed) 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.

Place, publisher, year, edition, pages
Ecological Society of America, 2022
Keywords
alternative states, C:P ratio, Daphnia, ecological stoichiometry, food quality, mesocosm experiment, paradox of energy enrichment, plant-herbivore, temperature, warming
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-124874 (URN)10.1002/ecy.3674 (DOI)000780007500001 ()2-s2.0-85127759512 (Scopus ID)
Funder
Knut and Alice Wallenberg Foundation, 016.0083Swedish Research Council, 621-2010-5316
Note

Originally included in thesis in manuscript form.

Available from: 2016-08-29 Created: 2016-08-29 Last updated: 2024-07-02Bibliographically approved
Uszko, W., Diehl, S. & Wickman, J. (2020). Fitting functional response surfaces to data: a best practice guide. Ecosphere, 11(4), Article ID e03051.
Open this publication in new window or tab >>Fitting functional response surfaces to data: a best practice guide
2020 (English)In: Ecosphere, ISSN 2150-8925, E-ISSN 2150-8925, Vol. 11, no 4, article id e03051Article in journal (Refereed) Published
Abstract [en]

Describing how resource consumption rates depend on resource density, conventionally termed "functional responses," is crucial to understanding the population dynamics of trophically interacting organisms. Yet, accurately determining the functional response for any given pair of predator and prey remains a challenge. Moreover, functional responses are potentially complex surfaces in multidimensional space, where resource density is only one of several factors determining consumption rates. We explored how three sources of error can be addressed in the design and statistical analysis of functional response experiments: ill-chosen spacing of prey densities, heteroscedastic variance in consumption rates, and non-independence of parameters of the function describing prey consumption in relation to prey density and additional environmental factors. We generated extensive, virtual data sets that simulated feeding experiments in which both prey density and environmental temperature were varied, and for which the true, deterministic functional response surface was known and realistic variance had been added. We compared eight different methods of functional response fitting, one of which stood out as best performing. We subsequently tested several conclusions from the simulation study against experimental data of zooplankton feeding on algae across a broad range of temperatures. We summarize our main findings in three best practice guidelines for the experimental estimation of functional response surfaces, of which the second is the most important: (1) space prey densities logarithmically, starting from very low densities; (2) log-transform prey consumption data prior to fitting; and (3) fit a multivariate functional response surface to all data (including all prey densities and other factors, in our case temperature) in a single step. We also observed that functional response surfaces were fitted more accurately and precisely than their component parameters. The latter occurred because parameter estimates were non-independent, which is an inevitable feature of fitting complex nonlinear functions to data: A given response surface can often be described with near-equal accuracy by multiple parameter combinations. We therefore conclude that fitted functional response models perform better at optimizing the fit of the overall response surface than at determining how component parameters, such as the attack rate or handling time, depend on environmental factors such as temperature.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2020
Keywords
data transformation, functional response, heteroscedasticity, Hill exponent, ingestion rate, parameter correlation, parameter estimation, prey density, temperature, type III
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-172511 (URN)10.1002/ecs2.3051 (DOI)000536583400024 ()2-s2.0-85084508099 (Scopus ID)
Funder
Swedish Research Council, 621-2010-5316
Available from: 2020-07-02 Created: 2020-07-02 Last updated: 2024-07-02Bibliographically approved
Cherif, M., Faithfull, C., Guo, J., Meunier, C. L., Sitters, J., Uszko, W. & Rivera Vasconcelos, F. (2017). An operational framework for the advancement of a molecule-to-biosphere stoichiometry theory. Frontiers in Marine Science, 4, Article ID 286.
Open this publication in new window or tab >>An operational framework for the advancement of a molecule-to-biosphere stoichiometry theory
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2017 (English)In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 4, article id 286Article in journal (Refereed) Published
Abstract [en]

Biological stoichiometry is an approach that focuses on the balance of elements in biological interactions. It is a theory that has the potential to causally link material processes at all biological levels—from molecules to the biosphere. But the lack of a coherent operational framework has so far restricted progress in this direction. Here, we provide a framework to help infer how a stoichiometric imbalance observed at one level impacts all other biological levels. Our framework enables us to highlight the areas of the theory in need of completion, development and integration at all biological levels. Our hope is that this framework will contribute to the building of a more predictive theory of elemental transfers within the biosphere, and thus, to a better understanding of human-induced perturbations to the global biogeochemical cycles.

Place, publisher, year, edition, pages
Lausanne: Frontiers Media S.A., 2017
Keywords
biological organization, biological stoichiometry, consumer-driven nutrient recycling, ecological theory, theory integration, growth-rate hypothesis, light:nutrient hypothesis
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-139395 (URN)10.3389/fmars.2017.00286 (DOI)2-s2.0-85029215410 (Scopus ID)
Available from: 2017-09-15 Created: 2017-09-15 Last updated: 2023-03-24Bibliographically approved
Uszko, W., Diehl, S., Englund, G. & Amarasekare, P. (2017). Effects of warming on predator-prey interactions - a resource-based approach and a theoretical synthesis. Ecology Letters, 20(4), 513-523
Open this publication in new window or tab >>Effects of warming on predator-prey interactions - a resource-based approach and a theoretical synthesis
2017 (English)In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 20, no 4, p. 513-523Article in journal (Refereed) Published
Abstract [en]

We theoretically explore consequences of warming for predator-prey dynamics, broadening previous approaches in three ways: we include beyond-optimal temperatures, predators may have a type III functional response, and prey carrying capacity depends on explicitly modelled resources. Several robust patterns arise. The relationship between prey carrying capacity and temperature can range from near-independence to monotonically declining/increasing to hump-shaped. Predators persist in a U-shaped region in resource supply (=enrichment)-temperature space. Type II responses yield stable persistence in a U-shaped band inside this region, giving way to limit cycles with enrichment at all temperatures. In contrast, type III responses convey stability at intermediate temperatures and confine cycles to low and high temperatures. Warming-induced state shifts can be predicted from system trajectories crossing stability and persistence boundaries in enrichment-temperature space. Results of earlier studies with more restricted assumptions map onto this graph as special cases. Our approach thus provides a unifying framework for understanding warming effects on trophic dynamics.

Keywords
Carrying capacity, consumer-resource interaction, Daphnia, enrichment, functional response, rsistence, predator-prey interaction, stability, temperature, warming
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-133190 (URN)10.1111/ele.12755 (DOI)000397100900013 ()2-s2.0-85014593644 (Scopus ID)
Available from: 2017-04-13 Created: 2017-04-13 Last updated: 2024-07-02Bibliographically approved
Uszko, W. (2016). Effects of warming and nutrient enrichment on feeding behavior, population stability and persistence of consumers and their resources. (Doctoral dissertation). Umeå: Umeå University
Open this publication in new window or tab >>Effects of warming and nutrient enrichment on feeding behavior, population stability and persistence of consumers and their resources
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
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.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2016. p. 27
Keywords
consumer-resource, Daphnia, functional response, nutrient enrichment, parameter estimation, persistence, plankton, predator-prey, stability, temperature, type II, type III, warming
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-124876 (URN)978-91-7601-544-5 (ISBN)
External cooperation:
Public defence
2016-09-20, Lilla Hörsalen (KB3A9), KBC, Umeå University, Umeå, 09:30 (English)
Opponent
Supervisors
Available from: 2016-08-30 Created: 2016-08-29 Last updated: 2024-07-02Bibliographically approved
Liess, A., Faithfull, C., Reichstein, B., Rowe, O., Guo, J., Pete, R., . . . Francoeur, S. N. (2015). Terrestrial runoff may reduce microbenthic net community productivity by increasing turbidity: a Mediterranean coastal lagoon mesocosm experiment. Hydrobiologia, 753(1), 205-218
Open this publication in new window or tab >>Terrestrial runoff may reduce microbenthic net community productivity by increasing turbidity: a Mediterranean coastal lagoon mesocosm experiment
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2015 (English)In: Hydrobiologia, ISSN 0018-8158, E-ISSN 1573-5117, Vol. 753, no 1, p. 205-218Article in journal (Refereed) Published
Abstract [en]

Terrestrial runoff into aquatic ecosystems may have both stimulatory and inhibitory effects, due to nutrient subsidies and increased light attenuation. To disentangle the effects of runoff on microbenthos, we added soil to coastal mesocosms and manipulated substrate depth. To test if fish interacted with runoff effects, we manipulated fish presence. Soil decreased microphytobenthic chlorophyll-a per area and per carbon (C) unit, increased microbenthic phosphorous (P), and reduced microbenthic nitrogen (N) content. Depth had a strong effect on the microbenthos, with shallow substrates exhibiting greater microbenthic net ecosystem production, gross primary production, and community respiration than deep substrates. Over time, micobenthic algae compensated for deeper substrate depth through increased chlorophyll-a synthesis, but despite algal shade compensation, the soil treatment still appeared to reduce the depth where microbenthos switched from net autotrophy to net heterotrophy. Fish interacted with soil in affecting microbenthic nutrient composition. Fish presence reduced microbenthic C/P ratios only in the no soil treatment, probably since soil nutrients masked the positive effects of fish excreta on microbenthos. Soil reduced microbenthic N/P ratios only in the absence of fish. Our study demonstrates the importance of light for the composition and productivity of microbenthos but finds little evidence for positive runoff subsidy effects.

Keywords
Bacteria, Dissolved organic carbon (DOC), Enclosure experiment, Microbenthos, Nutrient subsidy, Terrestrial subsidy
National Category
Ecology Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-106254 (URN)10.1007/s10750-015-2207-3 (DOI)000354194600014 ()2-s2.0-84939951034 (Scopus ID)
Available from: 2015-07-13 Created: 2015-07-09 Last updated: 2023-03-24Bibliographically approved
Uszko, W., Diehl, S., Pitsch, N., Lengfellner, K. & Müller, T. (2015). When is a type III functional response stabilizing?: theory and practice of predicting plankton dynamics under enrichment. Ecology, 96(12), 3243-3256
Open this publication in new window or tab >>When is a type III functional response stabilizing?: theory and practice of predicting plankton dynamics under enrichment
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2015 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 96, no 12, p. 3243-3256Article in journal (Refereed) Published
Abstract [en]

The curvature of generalized Holling type functional response curves is controlled by a shape parameter b yielding hyperbolic type II (b = 1) to increasingly sigmoid type III (b > 1) responses. Empirical estimates of b vary considerably across taxa. Larger consumer-resource body mass ratios have been suggested to generate more pronounced type III responses and therefore to promote dynamic stability. The dependence of consumer-resource stability on b has, however, not been systematically explored, and the accurate empirical determination of b is challenging. Specifically, the shape of the functional response of the pelagic grazer Daphnia feeding on phytoplankton, and its consequences for stability, remain controversial. We derive a novel analytical condition relating b to local stability of consumer-resource interactions and use it to predict stability of empirically parameterized models of Daphnia and phytoplankton under enrichment. Functional response parameters were experimentally derived for two species of Daphnia feeding separately on single cultures of two different phytoplankton species. All experimentally studied Daphnia-algae systems exhibited type III responses. Parameterized type III responses are predicted to stabilize the modeled Daphnia-phytoplankton dynamics in some species pairs but not in others. Remarkably, stability predictions differ depending on whether functional response parameters are derived from clearance vs. ingestion rates. Accurate parameter estimation may therefore require fitting to both rates. In addition, our estimates of b for filter-feeding Daphnia are much smaller than predicted for actively hunting predators at similar consumer-resource body mass ratios. This suggests that the relationship between functional response shape and body mass ratios may vary with predation mode.

Place, publisher, year, edition, pages
John Wiley & Sons, 2015
Keywords
body size, clearance rate, consumer-resource dynamics, Daphnia, filter feeder, functional response, gestion rate, parameter estimation, phytoplankton-zooplankton dynamics, stability
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-114583 (URN)10.1890/15-0055.1 (DOI)000367287900012 ()2-s2.0-84953207347 (Scopus ID)
External cooperation:
Available from: 2016-02-16 Created: 2016-01-25 Last updated: 2024-07-02Bibliographically approved
Koizumi, S., Uszko, W., Karlsson, J. & Byström, P.Antagonistic responses to warming and browning in fish-size structure and population abundance.
Open this publication in new window or tab >>Antagonistic responses to warming and browning in fish-size structure and population abundance
(English)Manuscript (preprint) (Other academic)
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-208048 (URN)
Available from: 2023-05-08 Created: 2023-05-08 Last updated: 2023-05-08
Uszko, W., Diehl, S., Englund, G. & Amarasekare, P.Effects of warming on predator-prey interactions: a resource-based approach and a theoretical synthesis.
Open this publication in new window or tab >>Effects of warming on predator-prey interactions: a resource-based approach and a theoretical synthesis
(English)Manuscript (preprint) (Other academic)
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-124873 (URN)
External cooperation:
Available from: 2016-08-29 Created: 2016-08-29 Last updated: 2024-07-02
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