Dr Isabel Smallegange - Associate Professor of Population Biology

General

My team and I (see InDEED team tab) research how ecological and evolutionary processes interact to determine the fluctuations of populations. Our research falls within three themes: functional trait demography, eco-evolutionary dynamics and developmental plasticity (see Research tab). To develop and test our hypotheses we use laboratory experiments on mites, statistical analysis of data and the construction and analysis of demographic models. We do not only apply our methods to small (laboratory) organisms like bulb mites (Rhizoglyphus robini) and beach hoppers (Orchestia gammarellus), but also to marine megafauna populations of rays, reef sharks and sea turtles.

A self-recorded 15 min talk on my recent paper on marine megafauna life history under environmental change:
Smallegange IM, Flotats Avilés M, Eustache K. 2020. Unusually paced life history strategies of marine megafauna drive atypical sensitivities to environmental variability. Frontiers in Marine Science 7:597492 https://doi.org/10.3389/fmars.2020.597492.

Podcast

► Population Biology & Eco-Evolutionary Dynamics From Mites to Manta Rays with Isabel Smallegange - Episode 9 of The Human Odyssey

Recruitment

If you are a quantitatively driven mind with interests in eco-evolutionary dynamics, life history, demography, or related topics, please contact me to discuss potential graduate and postdoc opportunities in my group.

In particular, if you have got a project in mind that you would like to develop in my group, please contact me with a brief project proposal, CV and list of funding themes that you are considering for this project (e.g. Marie Curie, NWO-VENI).

InDEED: Integrating Development, Ecological and Evolutionary Dynamics

The team

The team consists of a diverse group of biologists that are interested in range of topics that include behavioural ecology, eco-evolutionary dynamics, life history theory, energy budget theory, and demography. Each year we have several Bachelor and Master students working in the lab. Prospective students, please check out the DEB-IPM project page and the alumni pages for an overview of current and previous projects (and publications that resulted from these projects).

Isabel Smallegange (team leader)

My research aims at developing a mechanistic framework to link ecology and evolution on the basis of the processes that drive the dynamics of heritable life history traits. I focus on understanding the maintenance and evolution of male dimorphism and the role of harvesting and environmental change in experimental and field populations. FUNDING: MacGillavry Fellowship (2013 - 2018), MEERVOUD (2014 - 2018) and VIDI (2015 - 2020) (NWO).

Flor Rhebergen (PhD student)

A PhD project by Flor Rhebergen investigating how harvesting and environmental variability affect the joint dynamics of life history traits and population biomass dynamics of 'fast' Rhizoglyphus robini and 'slow' Naiadacarus arboricola populations in the lab and in the field. FUNDING: VIDI Fellowship (awarded to I.M. Smallegange).

Mark Rademaker (PhD student at the Royal Netherlands Institute for Sea Research and IBED-UvA)

Mark is doing his PhD under the daily supervision of Anieke van Leeuwen on fish ecology using an empirical-theoretical approach. The aim is to understand how changing climate conditions and human impacts affect the dynamics of marine fish stocks. Both Mark and Anieke are based at the Royal Netherlands Institute for Sea Research, and Mark will defend his thesis at the University of Amsterdam.

Kim Eustache (PhD student at CRIOBE / Perpignan University and IBED-UvA)

Kim is doing a joint doctorate PhD between the University of Perpignan / CRIOBE, where she is supervised by Serge Planes , and the University of Amsterdam, where she is supervised by Isabel Smallegange, on recruitment in black tip reef sharks (Carcharhinus melanopterus) off the coast of the island of Moorea in French Polynesia. The aim is to understand the black tip reef sharks' genetics and demography to improve local conservation strategies.

Marjolein Toorians (visiting PhD student University of British Columbia, Canada)

Marjolein is doing her PhD under the direct supervision of Jonathan Davies on the role of transmission in the disease-diversity relationship and reservoir dynamics. She will visit the lab in 2021 to work on a multi-host reservoir model including evolutionary history.

Collaborators

We have collaborated, and continue to collaborate, with many excellent scientists from around the world. Currently we have active collaborations with:

• University of British Columbia (CA) - Jonathan Davies: Transmission, disease-diversity relationship and reservoir dynamics.
• CRIOBE (France/Polynesia) – Serge Planes:  Recruitment and conservation of sharks.
• UvA Faculty of Humanities (NL) - Annemie Ploeger: developmental plasticity and human and non-human animals.
• University of Vigo (Spain) – Rula Domínguez:  Prey preference of marine predators.
• Wageningen University (NL) – Gerlinde de Deyn: mites and N₂O emission
• NIOZ (NL) – Anieke van Leeuwen:  Size-structured fish ecology under anthropogenic pressures.
• NIOZ (NL) – Jan van Gils:  Demography of red knots.

Recruitment and opportunities

If you are a quantitatively driven mind with interests in eco-evolutionary dynamics, life history, demography, or related topics, please contact me to discuss potential graduate and postdoc opportunities in my group.

In particular, if you have got a project in mind that you would like to develop in my group, please contact me with a brief project proposal, CV and list of funding themes that you are considering for this project (e.g. Marie Curie, NWO-VENI).

Research conducted within the team falls within three themes.

Functional trait demography

Climate variability is increasing. How will this affect different plant and animal species? We are in great need of an integrative framework that allows ecologists to predict life history strategies (i.e. the different ways in which individuals trade-off resource investment into survival or reproduction) from functional traits: traits of individuals that inform on the performance of a population of plants or animals as a whole. Such a framework is important to inform conservation strategies. Our research takes the mechanistic underpinnings of biological variation as a starting point to extrapolate from life history strategies the responses of populations to future environmental changes. Our analyses are also part of the DEB-IPM project where we link functional life history traits to population response to environmental change.

Eco-evolutionary dynamics

How evolutionary changes (like shifts in genotype and phenotype frequencies) and ecological changes (like the size, composition and growth of an animal or plant population) affect each other is a topic of intense and growing investigation in biology. Why? Because for a long time, ecologists ignored evolutionary processes as they were assumed to occur at much longer time scales (thousands to millions of years) compared to ecological processes (days to years). Vice versa, evolutionary biologists ignored ecological processes as these were assumed to occur at such short time scales that their effects would be unnoticeable at the long, evolutionary timescales. However, over the past decades, notions have changed and we now want to understand how ecological and evolutionary variables are both the drivers and the objects of change. Our research aims at formulating and testing predictions on eco-evolutionary population responses to environmental change using demographic models, long-term population experiments with bulb mites in the lab, and simulations on field data collected for a wide range of species.

Developmental plasticity

Developmental plasticity, whereby a specific input during an individual’s development produces a lasting alteration in phenotype, has been well-documented in human and non-human animals. It is studied by both evolutionary biologists and researchers studying human health. However, there is still little cross-disciplinary understanding of developmental plasticity. Two types of developmental plasticity can be recognized: predictive and constraints-induced developmental plasticity. Importantly, developmental plasticity can alter the direction of evolutionary change to the extent that phenotypic variation derived from development becomes encoded in the genome. We aim to unravel the mechanisms and drivers of developmental plasticity using the two male morphs of the bulb mite as our model system.

What is the DEB-IPM project about?

How can we predict how populations respond to the ever greater changes in their environment? Within this project, we want to know which characteristics of organisms relate to population responses to environmental change. One way to find out is to analyse life history patterns using demographic models. However, depending on whether you model individual life histories from phenomenological descriptions (Salguero-Gomez et al. 2016; Paniw et al. 2018; Capdevila et al 2020) or from mechanistic descriptions using energy budget models (Smallegange et al. in press; Smallegange & Berg 2019), different predictions are obtained.

The DEB-IPM project aims to (i) unravel if energy budget descriptions of individual life histories consistently return different predictions on population responses to environmental change compared to when individual life histories are represented by statistical functions, (ii) understand why that is the case, and (iii) identify the most accurate way to predict population responses to novel environmental change. To this end, we support Bachelor, Master and PhD student projects in which students answer their own research questions, while at the same time expanding the DEB-IPM database to ultimately conduct large, cross-taxonomical life history analyses.

What is a DEB-IPM?

Integral projection models (IPMs) have emerged as a powerful tool to investigate population-level processes from an individual-level perspective, partly because the demographic processes of growth, survival and reproduction are estimated using flexible and easy-to-use phenomenological methods such as regression models (Smallegange & Coulson 2013). The downside of these regression models, however, is that they lack a mechanistic representation of the biological processes that give rise to observed survival, growth and reproduction. The DEB-IPM (Smallegange et al. 2017) explicitly incorporates an energetic description of growth and reproduction into IPMs. IPMs, and also DEB-IPMs, can be analysed using tools from demography. This will allow researchers to investigate ecological and evolutionary patterns such as population dynamics, geographic distributions or evolution of life-history strategies, from an energy budget perspective on demographic rates, which has traditionally been tackled by using the mathematically more challenging physiological structured population models (de Roos & Persson 2013).

DEB-IPM database

The number of species for which we have collected data to parameterize a DEB-IPM is increasing, and are collated in an excel file: DEB-IPM project. Database of DEB-IPM model parameters.

Who is involved

Several projects are ongoing:

• Mark Rademakers (PhD student at the NIOZ and IBED/UvA): Can energy budget strategies forecast population growth in fish in temporally autocorrelated environments?
• Kim Eustache (PhD student at CRIOBE and IBED/UvA): Study of the effects of yearling, juvenile and adult survival on blacktip reef shark (Carcharhinus melanopterus) population demography.
• Dóra Vig (MSc student at Utrecht University): Comparison of population-level life-history patterns of invasive marine species, using dynamic energy budget integral projection models.
• Isabel Smallegange (group leader): The role of developmental plasticity in population persistence.

Do you want to be involved?

If you are a quantitatively driven mind with interests in life history theory, demography, eco-evolutionary dynamics, or related topics, please contact me to discuss potential graduate or postdoc opportunities in my group. Students: Below is a list of current and past student projects conducted within the DEB-IPM project. Contact me to discuss research questions you would like to tackle. Postdoctoral researchers: If you have got a project in mind that you would like to develop in my group, please contact me with a brief project proposal, CV and list of funding themes that you are considering for this project (e.g. Marie Curie, NWO-VENI).

Past DEB-IPM student projects:

• Sophie Timmerman: On the paradox in dynamic energy budget population models (2019).

• Gavin Jansen: Predicting changes in population dynamics using stochastic demographic models (2018).
• Tom Hopman: An analysis of life-history patterns in the fast-slow continuum using dynamic energy budget theory (2018).
• Naomi Eeltink: Predicting life history patterns across the fast-slow continuum: A cross-level test using the Dynamic Energy Budget-Integral Projection Model (DEB-IPM) (2017).
• Marjolein Toorians: her BSc project is part of the paper Smallegange et al. (2017) (see below).

Scientific papers of the DEB-IPM project

• Smallegange IM, Flotats Avilés M, Eustache K. in press. Unusually paced life history strategies of marine megafauna drive atypical sensitivities to environmental variability. Frontiers in Marine Science.

• Smallegange IM, Berg M. 2019. A functional trait approach to identifying life history patterns in stochastic environments. Ecology and Evolution 9: 9350-9361
• Smallegange IM, Ens HM. 2018. Trait-based predictions and responses from laboratory mite populations to harvesting in stochastic environments. Journal of Animal Ecology 87: 893-905
• Smallegange IM, Caswell H, Toorians MEM, de Roos AM. 2017. Mechanistic description of population dynamics using dynamic energy budget theory incorporated into integral projection models. Methods in Ecology and Evolution 8: 146-154

Popular science on the DEB-IPM project

• Podcast: Population Biology & Eco-Evolutionary Dynamics From Mites to Manta Rays with Isabel Smallegange - Episode 9 of The Human Odyssey

• Smallegange IM, Berg MP. 2019. A slow pace of life makes animals more sensitive to unpredictable climate variations. Amsterdam Science 11:3.
• Smallegange IM. Big data also need big concepts. Blog post September 2019.

References

• Capdevila P, Beger M, Blomberg SP, Hereu B, Linares C, Salguero-Gómez R, in press. Longevity, body dimension and reproductive mode drive differences in aquatic versus terrestrial life history strategies. Functional Ecology.

• Paniw M, Ozgul A & Salguero‐Gómez R. (2018). Interactive life‐history traits predict sensitivity of plants and animals to temporal autocorrelation. Ecology Letters 21: 275–286.
• de Roos AM, Persson L. (2013) Population and Community Ecology of Ontogenetic Development (Monographs in Population Biology, 51). Princeton University Press, Princeton, NJ, USA.
• Salguero-Gómez R, Jones OR, Jongejans E, Blomberg SP, Hodgson DJ, Mbeau-Ache C. et al. (2016). Fast–slow continuum and reproductive strategies structure plant life-history variation worldwide. Proc. Natl Acad. Sci. 113: 230–235.
• Smallegange IM, Coulson T (2013). Towards a general, population-level understanding of eco-evolutionary change. Trends in Ecology & Evolution 28: 143-148.
• Smallegange IM, Berg M. (2019). A functional trait approach to identifying life history patterns in stochastic environments. Ecology and Evolution 9: 9350-9361
• Smallegange IM, Caswell H, Toorians MEM & de Roos AM (2017). Mechanistic description of population dynamics using dynamic energy budget theory incorporated into integral projection models. Methods in Ecology and Evolution 8: 146–154.
• Smallegange IM, Flotats Avilés M, Eustache K. in press. Unusually paced life history strategies of marine megafauna drive atypical sensitivities to environmental variability. Frontiers in Marine Science.

Courses that we teach in:

• ‘Toekomstperspectief voor de Aarde’ (convener and lecturer); 6 EC BSc course
• Grand Challenges of Human-Ecosphere Interactions (theme convener and lecturer); 6 EC MSc course
• Current Trends in Ecology & Evolution (lecturer); 6 EC MSc course
• Psychobiology Year 2 Review (lecturer); 6 EC BSc course
• TESLA interdisciplinary MSc minor (science, business, society) (project supervisor); 30 EC 

Information for prospective students

The alumni page provides an overview of previous student projects. Please contact me if you are interested in doing a research project on behavioural ecology, population biology, demography, either using experimental methods or theoretical tools (or both). 

We are committed not only to acquiring knowledge, but also to disseminating it. We periodically publish general public outputs (e.g. in Amsterdam Science, or in blogs of the peer-reviewed journals Oikos, Journal of Animal Ecology  Functional Ecology, and of the Rapid Ecology community, run events at primary schools, and discuss research with secondary school teachers.

► Podcast: Population Biology & Eco-Evolutionary Dynamics From Mites to Manta Rays with Isabel Smallegange - Episode 9 of The Human Odyssey

►Blog posts on our research, including inside stories, future plans and wild ideas
►Blog posts on the work / life balance
►Blog posts on on the actitivies of the UvA Faculty of Science Works Council, of which I am Chair

If you’d like us to come talk to you about ecology and evolution, climate change or developmental plasticity, please contact us.

Post Docs

Kathryn (Kat) Stewart

Kat investigated how alternative mating tactics arise and are maintained within species, employing experimental approaches that incorporated environmental and demographic parameters with population genetics. Her research interests pivot around the origins and maintenance of biodiversity, from the level of local adaptation and limiting gene flow in single landscapes, through the genetics of entire species' ranges, to understanding the causes of diversification of entire clades. FUNDING: VIDI Fellowship (awarded to I.M. Smallegange).

Jacques Deere

Jacques investigated, using the bulb mite ( Rhizoglyphus robini) as a study species, the influence of dispersal propensity on population size and structure, life histories and how these change with stochastic environments. 

Laura Gangoso

Laura won a Marie Curie Fellowship and was based in the group of Willem Bouten. In her Post Doc she studied the ecological and evolutionary consequences of predator-prey phenological match-mismatch driven by climate change using Eleonora's falcon as a study system. Interestingly, Eleonora's falcon has a genetically determined colour polymorphism that covaries with behavioural traits and, together with Isabel, she aimed to explore the eco-evolutionary dynamics of variation in this colour polymorphism using integral projection models.

PhD students

Tom van den Beuken

Many species exhibit two discrete male morphs: fighters and sneakers. Fighters are large and possess weapons that they use to kill rival males. Sneakers are small without weapons but can sneak matings. Tom's PhD research focused on finding out why such discrete morphs can coexist in single populations and what drivers underlie the expression of such dimorphisms. FUNDING: MacGillavry Fellowship (awarded to I.M. Smallegange).

Rula Domínguez

Rula is a marine biologist with a diverse professional experience in marine ecology and biological oceanography, ranging from fisheries acoustics of pelagic fish stocks, to rocky shore ecology, lately to zooplankton ecology. She is currently doing a PhD in ecophysiology of intertidal bivalves at the University of Vigo, Spain. In 2020, she visited my lab for several months, until the corona crisis forced her to return to Spain. We work on a project investigating how salinity stress impacts predation risk of bivalve species both endemic and invasive to the Vigo coast.

Jacques Deere

Jacques investigated, using the bulb mite ( Rhizoglyphus robini) as a study species, the influence of dispersal propensity on population size and structure, life histories and how these change within stochastic environments.

MSc and BSc student projects that resulted in publications

One of the things I am most proud of about my research group is the fact that Master students at very early stages of their careers have completed projects that have gone on to be published in the international, peer-reviewed journals. Papers that resulted from their work are given below.

Marta Flotats Aviléz & Kim Eustache

Smallegange IM, Flotats Avilés M, Eustache K. 2020. Unusually paced life history strategies of marine megafauna drive atypical sensitivities to environmental variability. Frontiers in Marine Science 7:597492

Logan Stockwell

van den Beuken TPG, Stockwell L, Smallegange IM. 2019. Et tu, brother? Kinship and increased nutrition lower cannibalism incidence in male bulb mites. Animal Behaviour  152: 45-52

Roos Draaijer

Stewart KA, Draaijer R, Kolasa MR, Smallegange IM. 2019. The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics. BMC Evolutionary Biology 19:58

Chris Duinmeijer

van den Beuken TPG, Duinmeijer CC, Smallegange IM. 2019. Costs of weaponry: unarmed males sire more offspring than armed males in a male-dimorphic mite. Journal of Evolutionary Biology 32: 153-162

Hedwig Ens

Smallegange IM, Ens HM. 2018. Trait‐based predictions and responses from laboratory mite populations to harvesting in stochastic environments. Journal of Animal Ecology 87: 893-905.

Rianne Fernandes en Jasper Croll

Smallegange IM, Fernandes RE, Croll JC. 2018. Population consequences of individual heterogeneity in life histories: overcompensation in response to harvesting of alternative reproductive tactics. Oikos 127: 738-749 doi: 10.1111/oik.04130

Croll JC, Egas M, Smallegange IM. 2019. An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics. Journal of Animal Ecology 88: 11-23.

Marjolein Toorians

Smallegange IM, Caswell H, Toorians, MEM, de Roos, AM. 2017. Mechanistic understanding of population dynamics using dynamic energy budget theory incorporated into integral projection models. Methods in Ecology and Evolution 8: 146-154

Isabelle van der Ouderaa

Smallegange IM,  van der Ouderaa IBC, Tibiriça Y.  2016. The effect of yearling, juvenile and adult survival on reef manta ray (Manta alfredi) demography. PeerJ 4:e2370

Debbie Leigh

Leigh DM, Smallegange IM.2014. Effects of variation in nutrition on male morph development in the bulb mite Rhizoglyphus robini. Experimental and Applied Acarology 64: 159-170.

Erika Dawson

Dawson, E.H., Chittka, L. 2012. Conspecific and Heterospecific Information Use in Bumblebees. PLoS ONE 7(2): e31444. doi:10.1371/journal.pone.0031444

Naomi Thorne

Smallegange IM, Charalambous M, Thorne N. 2012. Fitness trade-offs and the maintenance of alternative male morphs in the bulb mite (Rhizoglyphus robini). Journal of Evolutionary Biology 25:972-980.

Ben Godsall

Godsall B, Smallegange IM. 2011. Assessment games in the mangrove tree-dwelling crab, Selatium brockii (De Man, 1887). Crustaceana 84:1697-1718.

Toos van Noordwijk

Smallegange IM, van Noordwijk CGE, van der Meer J, van der Veer HW. 2009. Spatial distribution of shore crab Carcinus maenas in an intertidal environment in relation to their morphology, prey availability and competition. Marine Ecology Progress Series 392:143-155.

Bert Hidding

Smallegange IM, Hidding B, Eppenga JMA, van der Meer J. 2008. Optimal foraging and risk of claw damage: how flexible are shore crabs in their prey size selectivity? Journal of Experimental Marine Biology and Ecology 367:157-163.

Ralf Kurvers

Smallegange IM, van der Meer J, Kurvers RHJM. 2006. Disentangling interference competition from exploitative competition in a crab-bivalve system using a novel experimental approach. Oikos 113:157-167.

Other student projects

• Marta Flotats Avilés: Assessing the impact of tourism on green turtle (Chelonia mydas) at Apo Island, the Phillipines (2020)
• Adam Zeeman: The role of adaptive developmental plasticity in maintaining polyphenism in cooperatively breeding societies (2020)
• Sophie Timmerman: On the paradox in dynamic energy budget population models (2019)
• Gavin Jansen: Predicting changes in population dynamics using stochastic demographic models (2018)
• Tom Hopman: An analysis of life-history patterns in the fast-slow continuum using dynamic energy budget theory (2018)
• Lars Schoen: The maintenance of polyphenism: sexual selection or energy budget limitations? A case study in acarid mites (2018)
• Johannes Meka: Temperature-dependent differences in individual behaviour and swimming performance in Atlantic mollies (Poecilia mexicana) reared in near-identical conditions (2018)
• Tim van Gorkum: Round and Round We Go: The role of eco-evolutionary feedbacks in population dynamics: 
  from alternative phenotype expression to demography and back (2018)
• Naomi Eeltink: SPredicting life history patterns across the fast-slow continuum: A cross-level test using the Dynamic Energy Budget-Integral Projection Model (DEB-IPM) (2017)
• Logan Stockwell: Conspecific killing and kin recognition in the bulb mite, Rhizoglyphus robini (2017)
• Hidde de Graaf: Male morph development of Rhizoglyphus robini under intrasexual competitive pressure (2017)
• Felicia Rook: Ways to reduce foraging stress in captive, non-human great apes (2017)
• Daniela Cueva: Non trophic interactions between ecosystem engineers (2017)
• Chris Duinmeijer: Sperm competition between male morphs of a male-dimorphic bulb mite (Rhizoglyphus robini) (2017)
• Charlotte Gredall: Investigating male and female fecundity as a consequence of juvenile somatic state in the developmentally plastic bulb mite, Rhizoglyphus robini (2017)
• Daphne Vink: The role of eco-evolutionary feedbacks in population dynamics: from alternative phenotype expression to demography and back (2017)
• Linde de Herder: Causes and consequences of calling site selection in male túngara frogs (Engystomops pustulosus) (2016)
• Ilona van den Berg: The effects of distinct dispersal life-histories in population models (2016)
• Tomos Potter: The impact of dispersal on population-level eco-evolutionary dynamics (2015)
• TIm van der Meer: Breeding diet and prey selection of African crowned eagles (Stephanoaetus coronatus) in urban areas of KwaZulu-Natal, South Africa (2015)
• Rianne Fernandes: Selection against fighter leads to a counterintuitive response, in dimorphic mite species the bulb mite (2015)
• Jasper Croll: How cannibalism influences the existence of alternative reproductive phenotypes (2015)
• Lars Kramer: The interplay between individual life history and population dynamics (2015)
• Hedwig Ens: "The effects of environmental noise on the population dynamics of harvested populations" (2012)
• Robbie L'Anson Price: "Pharaoh's Ants and foraging signals" (2012)
• Mike Wilson: "Alternative reproductive phenotype expression in the bulb mite Rhizoglyphus robini (Claparède): the influence of genetic variation" (2011)
• Rebecca O'Brien: "Size does matter: Contest dynamics in fiddler crabs, Uca perplexa" (2011) 
• Idde Lijnse: "The effect of intraspecific competition on prey selection in great tits (Parus major) and shore crabs (Carcinus maenas)" (2003)