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Application of Metabolic Theory in Models for Growth of Individuals and Populations
Linköpings universitet, Institutionen för fysik, kemi och biologi, Biologi. Linköpings universitet, Tekniska fakulteten. School of Bioscience, University of Skövde.ORCID-id: 0000-0003-0097-1379
2024 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

Metabolic theories in ecology interpret ecological patterns at different levels (individuals, populations, communities) through the lens of metabolism, often applying allometric scaling with rates of energy use described as power functions of body mass. However, the application of metabolic theory at higher levels requires a sound theory for metabolism at the individual level.

In this thesis, metabolic theory has been developed and applied in three different contexts; 1) growth of individual organisms under food limitation, 2) life-history theory for age and size at maturity for individual organisms, and 3) population growth of marine mammals exposed to bioaccumulative toxicants through their diet.

In the first context, a new mechanistic model for individual growth was developed, based on an energy balance that expresses growth as the net result of energy assimilation from food and various metabolic costs. The model can account for effects of body composition and cellular-level growth patterns, but foremost it considers a potential trade-off between regulated maintenance and growth under food limitation. The model was successfully calibrated and validated against empirical data for an insect (house cricket) under both unlimited and limited food conditions. Interestingly, the empirical calibration indicated that the energy per unit body mass that an organism allocates to maintenance of body structures may increase as the organism grows and may also be upregulated under food limitation.

In Paper I, the maintenance-growth model (MGM), is presented, derived and demonstrated via numerical simulations and comparisons with available growth data. In Paper II and III, MGM is calibrated and evaluated against collected data for house crickets growing under unlimited and restricted food supply, respectively.

In the second context (Paper IV), it was investigated how models for individual growth and mortality can be combined with life-history theory to model plastic responses in age and size at maturity under varying resource conditions. The new growth model (MGM) was implemented to account for the trade-off between somatic maintenance and growth. It was also investigated how life-history models that predict the occurrence of maturity are affected by the presence of an overhead threshold, a minimum size that organisms must reach in order to mature and exceed in order to reproduce. It was found that the existence of an overhead threshold, that previously has been considered to be a crucial assumption for predicting realistic reaction norms for age and size at maturity, may not be crucial after all.

In the final context (Paper V), a model was developed for bioaccumulation of toxicants and their effects on survival rates, fertilities, age structure and population growth in marine mammals. Allometric scaling of biological rates were applied in the parametrisation of the model. The model was successfully calibrated and validated against empirical data for Baltic grey seals affected by PCB. The model could demonstrate that decreased female fertility (caused by a toxicant) may considerably increase bioaccumulation of the toxicant due to decreased offload from females to offspring.

sted, utgiver, år, opplag, sider
Linköping: Linköping University Electronic Press, 2024. , s. 68
Serie
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 2400
Emneord [en]
Metabolism, Metabolic rate, Allometric scaling, Somatic maintenance, Ontogenetic growth, Growth model, Food restriction, Insects, Life-history traits, Age at maturity, Size at maturity, Bioaccumulation, Toxicokinetics, Toxicodynamics, Population dynamics, Marine mammals
HSV kategori
Identifikatorer
URN: urn:nbn:se:liu:diva-207620DOI: 10.3384/9789180757379ISBN: 9789180757362 (tryckt)ISBN: 9789180757379 (digital)OAI: oai:DiVA.org:liu-207620DiVA, id: diva2:1897897
Disputas
2024-10-11, G110, G Building, University of Skövde, Skövde, 09:15 (engelsk)
Opponent
Veileder
Merknad

Funding agencies: The Swedish research council, grant number 2018-05523, Viltforskningsanslaget, Swedish Environmental Protection Agency, and the BONUS program BaltHealth (Art. 185).

2024-09-16: The thesis was first published online. The online published version reflects the printed version.

2024-09-30: The thesis was updated with an errata list which is also downloadable from the DOI landing page. Before this date the PDF has been downloaded 37 times.

Tilgjengelig fra: 2024-09-16 Laget: 2024-09-16 Sist oppdatert: 2024-09-30bibliografisk kontrollert
Delarbeid
1. A new flexible model for maintenance and feeding expenses that improves description of individual growth in insects
Åpne denne publikasjonen i ny fane eller vindu >>A new flexible model for maintenance and feeding expenses that improves description of individual growth in insects
2023 (engelsk)Inngår i: Scientific Reports, E-ISSN 2045-2322, Vol. 13, nr 1, artikkel-id 16751Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

Metabolic theories in ecology interpret ecological patterns at different levels through the lens of metabolism, typically applying allometric scaling to describe energy use. This requires a sound theory for individual metabolism. Common mechanistic growth models, such as 'von Bertalanffy', 'dynamic energy budgets' and the 'ontogenetic growth model' lack some potentially important aspects, especially regarding regulation of somatic maintenance. We develop a model for ontogenetic growth of animals, applicable to ad libitum and food limited conditions, based on an energy balance that expresses growth as the net result of assimilation and metabolic costs for maintenance, feeding and food processing. The most important contribution is the division of maintenance into a 'non-negotiable' and a 'negotiable' part, potentially resulting in hyperallometric scaling of maintenance and downregulated maintenance under food restriction. The model can also account for effects of body composition and type of growth at the cellular level. Common mechanistic growth models often fail to fully capture growth of insects. However, our model was able to capture empirical growth patterns observed in house crickets.

sted, utgiver, år, opplag, sider
Nature Publishing Group, 2023
HSV kategori
Identifikatorer
urn:nbn:se:liu:diva-202784 (URN)10.1038/s41598-023-43743-1 (DOI)001085340000017 ()37798309 (PubMedID)
Tilgjengelig fra: 2024-04-19 Laget: 2024-04-19 Sist oppdatert: 2024-09-16
2. A new mechanistic model for individual growth applied to insects under ad libitum conditions
Åpne denne publikasjonen i ny fane eller vindu >>A new mechanistic model for individual growth applied to insects under ad libitum conditions
2024 (engelsk)Inngår i: PLOS ONE, Vol. 19, nr 9Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

Metabolic theories in ecology interpret ecological patterns at different levels through the lens of metabolism, typically applying allometric power scaling laws to describe rates of energy use. This requires a sound theory for metabolism at the individual level. Commonly used mechanistic growth models lack some potentially important aspects and fail to accurately capture a growth pattern often observed in insects. Recently, a new model (MGM–the Maintenance-Growth Model) was developed for ontogenetic and post-mature growth, based on an energy balance that expresses growth as the net result of assimilation and metabolic costs for maintenance and feeding. The most important contributions of MGM are: 1) the division of maintenance costs into a non-negotiable and a negotiable part, potentially resulting in maintenance costs that increase faster than linearly with mass and are regulated in response to food restriction; 2) differentiated energy allocation strategies between sexes and 3) explicit description of costs for finding and processing food. MGM may also account for effects of body composition and type of growth at the cellular level. The model was here calibrated and evaluated using empirical data from an experiment on house crickets growing under ad libitum conditions. The procedure involved parameter estimations from the literature and collected data, using statistical models to account for individual variation in parameter values. It was found that ingestion rate cannot be generally described by a simple allometry, here requiring a more complex description after maturity. Neither could feeding costs be related to ingestion rate in a simplistic manner. By the unusual feature of maintenance costs increasing faster than linearly with body mass, MGM could well capture the differentiated growth patterns of male and female crickets. Some other mechanistic growth models have been able to provide good predictions of insect growth during early ontogeny, but MGM may accurately describe the trajectory until terminated growth.

sted, utgiver, år, opplag, sider
Public Library of Science, 2024
HSV kategori
Identifikatorer
urn:nbn:se:liu:diva-207754 (URN)10.1371/journal.pone.0309664 (DOI)
Merknad

Funding was provided by the Swedish research council, grant number 2018-05523

Tilgjengelig fra: 2024-09-20 Laget: 2024-09-20 Sist oppdatert: 2024-09-20bibliografisk kontrollert
3. A new mechanistic model for individual growth suggests upregulated maintenance costs when food is scarce in an insect
Åpne denne publikasjonen i ny fane eller vindu >>A new mechanistic model for individual growth suggests upregulated maintenance costs when food is scarce in an insect
2024 (engelsk)Inngår i: Ecological Modelling, ISSN 0304-3800, E-ISSN 1872-7026, Vol. 491, artikkel-id 110703Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

A growing animal ingests food from the environment and distributes the assimilated energy between chemical energy stored in synthesized biomass and energy spent on metabolic processes, including food processing, maintenance, activity and overhead costs for growth. Under food restriction, the growth rate is usually decreased. However, the extent of this reduction may be influenced by a potential trade -off with maintenance metabolism. The latter seems to be down-regulated under food restriction in some animals and up-regulated in others. Recently, the Maintenance-Growth Model (MGM) was developed for ontogenetic and post-mature growth, including several aspects not considered by common mechanistic growth models, most importantly the division of maintenance costs into non-negotiable and negotiable parts, where the latter can be up- or downregulated under food restriction. Using empirical data, MGM has been calibrated and successfully applied to an insect growing under ad libitum conditions. Here, the model is further calibrated to newly collected individual data for the same species growing under two different regimes of food restriction, complemented with previously collected data for food-limited cohorts. We find that two alternative model scenarios of MGM are able to generate rather good predictions of observed growth under food restriction, assuming either upregulated maintenance or decreased effective assimilation (assimilation minus energy spent on processing and searching food). We find the latter scenario least plausible, implying that the current study provides the first indication for the occurrence of upregulated maintenance in an insect species when food is scarce, an unexpected result that requires further investigation. The inclusion of maintenance regulation in MGM enables the new growth model to be used in the modelling of life-history dependent trade-offs between maintenance, growth and maturation for various other species.

sted, utgiver, år, opplag, sider
ELSEVIER, 2024
Emneord
Growth model; Metabolic rate; Maintenance; Food restriction; Insects; House cricket (Achetadomesticus)
HSV kategori
Identifikatorer
urn:nbn:se:liu:diva-203590 (URN)10.1016/j.ecolmodel.2024.110703 (DOI)001217619300001 ()
Merknad

Funding Agencies|Swedish research council [2018-05523]

Tilgjengelig fra: 2024-05-22 Laget: 2024-05-22 Sist oppdatert: 2024-09-16
4. Maternal Transfer and Long-Term Population Effects of PCBs in Baltic Grey Seals Using a New Toxicokinetic–Toxicodynamic Population Model
Åpne denne publikasjonen i ny fane eller vindu >>Maternal Transfer and Long-Term Population Effects of PCBs in Baltic Grey Seals Using a New Toxicokinetic–Toxicodynamic Population Model
2022 (engelsk)Inngår i: Archives of Environmental Contamination and Toxicology, ISSN 0090-4341, E-ISSN 1432-0703, Vol. 83, nr 4, s. 376-394Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

Empirical evidence has shown that historical exposure of polychlorinated biphenyls (PCBs) to Baltic grey seals not only severely affected individual fitness, but also population growth rates and most likely caused the retarded recovery rate of the depleted population for decades. We constructed a new model which we term a toxicokinetic–toxicodynamic (TKTD) population model to quantify these effects. The toxicokinetic sub-model describes in detail the bioaccumulation, elimination and vertical transfer from mother to offspring of PCBs and is linked to a toxicodynamic model for estimation of PCB-related damage, hazard and stress impacts on fertility and survival rates. Both sub-models were linked to a Leslie matrix population model to calculate changes in population growth rate and age structure, given different rates of PCB exposure. Toxicodynamic model parameters related to reproductive organ lesions were calibrated using published historical data on observed pregnancy rates in Baltic grey seal females. Compared to empirical data, the TKTD population model described well the age-specific bioaccumulation pattern of PCBs in Baltic grey seals, and thus, the toxicokinetic parameters, deduced from the literature, are believed to be reliable. The model also captured well the general effects of PCBs on historical population growth rates. The model showed that reduced fertility due to increased PCB exposure causes decreased vertical transfer from mother to offspring and in turn increased biomagnification in non-breeding females. The developed TKTD model can be used to perform population viability analyses of Baltic grey seals with multiple stressors, also including by-catches and different hunting regimes. The model can also be extended to other marine mammals and other contaminants by adjustments of model parameters and thus provides a test bed in silico for new substances.

HSV kategori
Identifikatorer
urn:nbn:se:liu:diva-207619 (URN)10.1007/s00244-022-00962-3 (DOI)
Merknad

Open access funding provided by University of Skövde. Funding was provided by Viltforskningsanslaget, Swedish Environmental Protection Agency (2021-00028) and the BONUS program BaltHealth (Art. 185). Mauritsson was partially supported by the Swedish research council, grant/award number 2018-05523.

Tilgjengelig fra: 2024-09-16 Laget: 2024-09-16 Sist oppdatert: 2024-09-16bibliografisk kontrollert

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