Our Research - Understanding the impact of environment on early development
Biology is breathtaking in its complexity. This is most apparent during the process of early development, where animals exhibit huge changes in their size, shape, and in the ways they function over different temporal and spatial scales. Phenomics, the acquisition of high-dimensional data at the scale of the whole organism, can capture this complexity. Its application to early development represents a step-change in the ways in which we can understand how animals work, as well as how they respond to an ever changing climate.
A warming world
How will global warming impact the development of aquatic life?
Human activity is causing our climate to warm at an unprecedented rate, with average temperatures predicted to reach 4.6°C above pre-industrial levels by the end of the century. Unsurprisingly, one of the most pressing questions of our time is how rising temperatures will impact animals occupying the natural environment. To address this question, we must start with the earliest, and often, most sensitive stage of life - the embryo. The temperature at which an animal develops can govern its health, survival and reproductive success, therefore it is crucial for us to study its impacts during this highly dynamic stages of life.
The technological requirements necessary to capture how changes in temperature shape this dynamic life stage are significant. The size, shape and ways in which an embryo functions change minute by minute, hour by hour, over the course of days, weeks or even months. Such effects may also be specific to particular species, populations or small groups of individuals. The ability to screen embryos at scale is necessary to provide a robust understanding of the sensitivity of early life stages to anthropogenic environmental change.
The above video was recorded using an automated bioimaging system in the EmbryoPhenomics facility at the University of Plymouth. The video shows a time-lapse of developing embryos of the wandering pond snail Radix balthica, at two ecologically realistic temperatures. As you can see, just a 5°C increase in rearing temperature changes how fast the animals develops, as well as a suite of other physiological processes.
To learn more about how acute and chronic changes in temperature, and a number of other environmental variables are impacting early life stages of aquatic animals, please see a list of the groups research below.
What’s the Latest?
Comparative phenomics and Heterochrony
by McCoy et al., 2023
Heterochrony, evolutionary changes in the timings of developmental events, is regarded as one of the main mechanisms of evolutionary change. Using EPTs, we found that high-dimensional changes in the developmental phenotype aligned with major sequence heterochronies in embryos of three freshwater snails. Reimaging the phenotype energy spectra allowed for continuous measurement of developmental changes, rather than only timings of discrete developmental events.
Characterising responses to multiple stressors
by Tills et al., 2023
Stressors in marine environments rarely act in isolation, therefore it is crucial that we measure how early life stages respond to multiple stressors. We investigated the response of an ecologically important marine invertebrate, the common prawn Palaemon serratus, to temperature and salinity stress using Energy Proxy Traits (EPTs). Complex developmental stage specific sensitivities highlighted both the complexity of phenotypic responses to multiple stressors, and limits of univariate approaches.
Thermal tolerance varies with life stage
by Truebano et al., 2018
Currently, a species sensitivity to temperature is predominantly based on adult performance, despite the fact that early life stages may be more vulnerable to thermal challenge. Here, we compared the sensitivity of different life history stages of an intertidal gastropod using methods, which incorporate the intensity and duration of heat stress, and used these to calculate upper critical thermal limits and sensitivity to temperature change. We found embryos to have a thermal limit 7°C lower than adults, indicating they’re more sensitive to elevated temperatures! This study highlights the need to assess early life stages to make more inclusive, robust predictions about the biological impacts of climate change.
Phenomics and Comparative Developmental Physiology
by McCoy et al., 2023
In this perspective, we explore the synergies between phenomics and Comparative Developmental Physiology (CDP). We ask what phenomics can contribute to CDP, as well as how embryonic development itself when viewed as a model system, may advance phenomics as an approach more generally. We suggest that phenomics of developing organisms may provide an effective scaffold with which to simultaneously address grand challenges in CDP , and in phenomics.
Automated measurement of heart rate and heart rate variability
by Ibbini et al., 2022
Heart function is a key component of whole organism physiology. A major limitation of many imaging methods used for measuring heart function is a lack of transferability between species. HeartCV is an open source Python package for the automated measurement of heart rate and heart rate variability in transparent animals, and is a applicable to a wide range of species. We demonstrate the applicability of this software to a range of experimental approaches.
Transcriptome response to predators
by Tills et al., 2018
It is known that kairomones, produced by predators, induce defenses in their prey. The question is how? Here, we examine the transcriptomic response to predator kairomones of two embryonic stages of a freshwater gastropod. We tested whether expression profiles were influenced by kairomones and whether this influence varied between stages. There were over 6k different transcripts between the two stages! 206 transcripts expressed were identified as being relating to muscle function, growth, and development, with a greater expression at the later embryonic stage. Do predator kiramones increase rates of muscle growth and development?
Interspecific differences in thermal phenomics
by McCoy et al., 2023
EPTs, while effective at characterising acute and chronic responses to elevated temperatures, remain untested in assessing sensitivities between species. In this study, we show that changes in EPT spectra in embryos of three species of freshwater snail exposed to chronic elevated temperatures, revealed marked differences in thermal sensitivities between species. Furthermore, differences in responses between different stages of development reflected ontogenetic changes in observable phenotypes, as well as temperature induced changes to the timings of developmental events.
Energy Proxy Traits - high-dimensional phenotyping of early development
by Tills et al., 2021
Energy Proxy Traits (EPTs) are a new approach to measuring the phenotype of developing animals. EPTs take fluctuations in pixels in video, and convert these into a spectrum of energy levels, thereby integrating all observable forms of biological movement visible in video data. Here, we demonstrate the biological relevance of this new holistic approach to phenotyping by measuring the thermal sensitivity of embryos of a freshwater snail, and relating these energy spectra to biological outcomes.
Sink or Swim? The effects of pH on jellyfish swimming
by Tills et al., 2016
Increased carbon dioxide in our atmosphere threatens to decrease the pH of our oceans, a process known as ocean acidification. Our knowledge of how ocean acidification affects the behaviour and growth of scyphozoan jellyfish is poor. In this study we investigated the effect of culture in reduced pH seawater on pulsation behaviour (as an index of swimming behaviour) and some key aspects of the morphology of ephyrae of the moon jellyfish. Pulsation rate was reduced and became more variable under acidified conditions. These sublethal effects maybe important factors in driving population persistence and abundance in the wild.
Published works
Journal articles
Haskett H, Gill L, Spicer JI, Truebano M. 2024. The embryonic thermal environment has positive but weak effects on thermal tolerance later in life in the aquatic invertebrate Gammarus chevreuxi. Marine Environmental Research, 195, 106350.
Amstutz A, Firth LB, Spicer JI, De Frenne P, Gómez-Aparicio L, Graae BJ, Kus S, Lindmo S, Orczewska A, Rodríguez-Sánchez F, Vagansbeke P, Vanneste T, Hanley ME. 2024. Taking sides? Aspect has limited influence on soil environment or litter decomposition in pan-European study of road side verges. Pedobiologia, 102, 150927.
Amstuz A, Firth LB, Foggo A, Spicer JI, Hanley ME. 2023. The north-south divide? Macroalgal functional trait diversity and redundancy varies with intertidal aspect. Annals of Botany.
McCoy JCS, Spicer JI, Rundle SD, Tills O. 2023. Comparative phenomics: a new approach to study heterochrony. Frontiers in Physiology, 14, 12370022.
McCoy JCS, Spicer JI, Tills O. 2023. Phenomics as an approach to Comparative Developmental Physiology. Frontiers in Physiology, 14, 1229500.
McCoy JCS, Spicer JI, Rundle SD, Tills O. 2023. A phenomics approach reveals interspecific difference in integrated developmental responses to chronic elevated temperatures. Journal of Experimental Biology, 226, jeb245612.
Clark, MS, Shabtay, A, Waters, E, Truebano, M. 2023. Organisms in a changing world. Cell Stress and Chaperones, 28, 441-443.
Collins, M, Clark, MS, Truebano, M. 2023. The environmental cellular response: the intertidal as a multistressor model. Cell Stress and Chaperones, 28, 467-475.
Tills O, Holmes LA, Quinn E, Everett T, Truebano M, Spicer JI. 2023. Phenomics enables measurement of complex responses of developing animals to global environmental drivers. Science of the Total Environment, 858, 159555.
Dwane C, Rezende EL, Tills O, Galindo J, Rolán-Alvarez E, Rundle S, Truebano M. 2023. Thermodynamic effects drive countergradient responses in the thermal performance of Littorina saxatilis across latitude. Science of the Total Environment, 863, 160877.
Ibbini Z, Spicer JI, Truebano M, Bishop J, Tills O. 2022. HeartCV: a tool for transferable, automated measurement of heart rate and heart rate variability in transparent animals. Journal of Experimental Biology, 225, jeb244729.
Wilson C, Spicer JI, Wyeth RC, McGaw IJ. 2022. Effect of Animal Stocking Density and Habitat Enrichment on Survival and Vitality of Wild Green Shore Crabs, Carcinus maenas, Maintained in the Laboratory. Animals, 12, 2970.
Garrard SL, Spicer JI, Thompson RC. 2022. Tyre particle exposure affects the heath of two key estuarine invertebrates. Environmental Pollution, 314, 120244.
McAndry C, Collins M, Tills O, Spicer JI, Truebano M. 2022. Regulation of gene expression during ontogeny of physiological function in the brackishwater amphipod Gammarus chevreuxi. Marine Genomics, 63, 100948.
Collins M, Truebano M, Spicer JI. 2022 Consequences of thermal plasticity for hypoxic performance in coastal amphipods. Marine Environmental Research, 177, 105624.
Amstutz A, Firth LB, Spicer JI, Hanley ME. 2021. Facing up to climate change: Community composition varies with aspect and surface temperature in the rocky intertidal. Marine Environmental Research, 172, 105482.
Tills O, Spicer JI, Ibbini Z. & Rundle SD. 2021 Spectral phenotyping of embryonic development reveals integrative thermodynamic responses. BMC Bioinformatics 22, 232.
Dwane C, Rundle SD, Tills O, Rezende EL, Galindo J, Rolán-Alvarez & Truebano M. 2021. Divergence in Thermal Physiology Could Contribute to Vertical Segregation in Intertidal Ecotypes of Littorina saxatilis. Physiol Biochem Zool 94, 353–365.
McCoy, JCS, Spicer, JI, Tills, O. & Rundle, S. D. 2020 ‘Both maternal and embryonic exposure to mild hypoxia influence embryonic development of the intertidal gastropod Littorina littorea’. Journal of Experimental Biology 223, 221895.
Bednaršek N, Feely RA, Beck MW, Alin SR, Siedlecki SA, Calosi P, Norton E, Saenger C, Štrus J, Greeley D, Nezlin, N.P., Roethler, M., & J.I. Spicer. 2020. Exoskeleton dissolution with mechanoreceptor damage in larval Dungeness crab related to severity of present-day ocean acidification vertical gradients. Science of the Total Environment, Available online 22 Jan 2020, 136610.
Small DP, Calosi P, Rastrick SPS, Turner LM, Boothroyd D, Widdicombe S & JI Spicer. 2020. The effects of elevated temperature and pCO2 on the energetics and haemolymph pH homeostasis in early benthic juvenile European lobster, Homarus gammarus (L.). Journal of Experimental Biology JEXBIO/2019/209221
Truebano M, Robertson S, Houston S, Tills O. & JI Spicer. 2020. Ontogeny of osmoregulation in the brackishwater amphipod Gammarus chevreuxi. Journal of Experimental Marine Biology and Ecology Volume 524, 151312
Arnberg M, Calosi P, Spicer JI, Taban IC, Bamber S, Westerlund S, Vingen S, Baussant T, Bechmann R & S. Dupont. 2018. Additive effects of oil and global stressors on two keystone marine invertebrates. Nature -Scientific Reports, Volume 8, pages 17380
Collins M, Tills O, Turner LM, Clark MS, Spicer JI, Truebano. 2018. Moderate reductions in dissolved oxygen may compromise performance in an ecologically-important estuarine invertebrate. Science of the Total Environment, 693:133444.
Tills O, Spicer JI, Grimmer A, Marini S, Jie VW, Tully E, & Rundle SD. 2018. A high-throughput and open-source platform for embryo phenomics. PLoS Biology, 16:e3000074.
Tills O, Truebano M, Feldmeyer B, Pfenninger M, Morgenroth H, Schell T, et al. 2018. Transcriptomic responses to predator kairomones in embryos of the aquatic snail Radix balthica. Ecology and Evolution. 201831:79–12.
Truebano M, Fenner P, Tills O, Rundle SD & Rezende EL. 2018. Thermal strategies vary with life history stage. Journal of Experimental Biology 221: jeb171629–5.
Truebano M, Tills O, Collins M, Clarke C, Shipsides E, Wheatley C, et al. 2018. Short-term acclimation in adults does not predict offspring acclimation potential to hypoxia. Scientific Reports, 8:1-9.
Schell T, Feldmeyer B, Schmidt H, Greshake B, Tills O, Truebano M, Rundle SD, Paule S, Ebersberger I & Pfenninger M. 2017. An annotated draft genome for Radix auricularia (Gastropoda, Mollusca). Genome Biology and Evolution 9: 585-592.
Rundle SD. & JI Spicer. 2016. Heterokairy: a neglected form of developmental plasticity? Biology Letters Invited review Volume 12: 20160509
Small DP, Calosi P, Boothroyd D, Widdicombe S & JI Spicer. 2016. Elevated pCO2 and temperature cause moult death syndrome in early benthic juvenile European lobsters, Homarus gammarus (L.) Marine Biology, Volume 163, pages 53-63.
Tills O, Sun X, Rundle SD, Heimbach T, Gibson T, Cartwright A, Palmer M, Rudin-Bitterli T & Spicer JI. 2016. Reduced pH affects pulsing behavior and body size in ephrae of the moon jellyfish, Aurelia aurita. Journal of Experimental Marine Biology and Ecology 480: 54-61.
Truebano M, Tills O & Spicer JI. 2016. Embryonic transcriptome of the brackishwater amphipod Gammarus chevreuxi. Marine Genomics 28: 5-6
Jarrold MD, Rodriguez-Romero A, Massamba-N’Siala G, Spicer JI & Calosi P. 2015. Multi-generational responses of a marine polychaete to a rapid change in environmental pCO2. Evolutionary Applications, Volume 9, pages 1082-1095.
Small DP, Calosi P, Boothroyd D, Widdicombe S. & Spicer JI. 2015. Stage-specific changes in physiological optima during larval development drive life history and population responses to complex climate changes in the European lobster, Homarus gammarus (L.). Physiological and Biochemical Zoology, Volume 88, pages 494-507.
Tills O, Truebano M & Rundle SD 2015. An embryonic transcriptome of the pulmonate snail Radix balthica. Marine Genomics 24: 259-260.
Rudin-Bitterli TS, Tills O, Spicer JI, Culverhouse PF, Wielhouwer EM, Richardson MK & Rundle SD. 2014. Combining motion analysis and microfluidics – A novel approach for detecting whole- animal responses to test substances. PloS ONE 9: e113235.
Arnberg M, Calosi P, Spicer JI, Tandberg AHS, Nilsen M, Westerlund S & Bechmann RK. 2013. Elevated temperature elicits greater effects than elevated pCO2 on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Marine Biology, Volume 160, pages 2037 – 2048.
Tills O, Bitterli T, Culverhouse P, Spicer JI & Rundle SD. 2013. A novel application of motion analysis for detecting stress responses in embryos at different stages of development. BMC Bioinformatics 14: 37.
Tills O, Rundle SD & Spicer JI. 2013. Variance in developmental event timing is greatest at low biological levels: implications for heterochrony. Biological Journal of the Linnean Society 110: 581-590.
Tills O, Rundle SD & Spicer JI 2013. Parent-offspring similarity in the timing of developmental events: an origin of heterochrony? Proceedings of the Royal Society B: Biological Sciences 280: 1769.
Bitterli T, Rundle SD and Spicer JI. 2012. Development of cardiovascular function in the marine gastropod Littorina obtusata (Linnaeus). Journal of Experimental Biology, Volume 215, pages 2327 – 2333.
Rundle SD, Smirthwaite JJ, Colbert MW & Spicer JI. 2011. Predation cues alter the timing of developmental events in gastropod embryos. Biology Letters, Volume 7, pages 285 – 287.
Spicer JI, Rundle SD & Tills O. 2011. Studying the altered timing of physiological events during development: It’s about time, or is it? Respiratory Physiology and Neurobiology 178: 3-12.
Tills O, Rundle SD, Culverhouse P, Spicer JI & Bitterli TS. 2011. Method and system for determining characteristics of an embryo and uses thereof. Patent, World Intellectual Property Organization.
Tills O, Rundle SD, Salinger M, Haun T, Pfenninger M & Spicer JI. 2011. A genetic basis for intraspecific differences in developmental timing? Evolution and Development 13: 542-548.
Findlay HS, Kendall MA, Spicer JI and Widdicombe S. 2010. Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Marine Biology (Berlin) Volume 157, pages 725 – 735.
Findlay HS, Kendall MA, Spicer JI & Widdicombe S. 2010. Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution. Estuaries, Coastal and Shelf Science, Volume 86, pages 675-682.
Mourabit S, Rundle SD, Spicer JI & Sloman KA. 2010. Alarm substance from adult zebrafish alters early embryonic development in offspring. Biology Letters, Volume 6, pages 525 – 528.
Tills O, Spicer JI & Rundle SD. 2010. Salinity-induced heterokairy in an upper-estuarine population of the snail Radix balthica. Aquatic Biology 9: 95-105.
Arnold KE, Findlay HS, Boothroyd D, Daniels CL and JI Spicer. 2009. Effect of hypercapnia-related acidification on the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences, Volume 6, pages 1747 – 1754.
Arnold KE, Wells C & Spicer JI. 2009. Effect of an insect juvenile hormone analogue, Fenoxycarb® on development and oxygen uptake by larval lobsters Homarus gammarus (L.). Comparative Biochemistry and Physiology C, Volume 149, pages 393 – 396.
Byrne RA, Rundle SD, Smirthwaite JJ. & Spicer JI. 2009. Embryonic rotational behaviour in the pond snail Lymnaea stagnalis; influence of environmental oxygen and developmental stage. Zoology- Analysis of Complex Systems, Volume 112, pages 471 – 477.
Egilsdottir H, Spicer JI & Rundle SD. 2009. The effect of CO2 acidified sea water and reduced salinity on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Marine Pollution Bulletin. Volume 58, pages 1187 – 1191.
Ellis RP, Bersey J, Rundle SD, Hall-Spencer, JM & Spicer JI. 2009. Subtle but significant effects of CO2 acidified sea water on embryos of the intertidal snail Littorina obtusata. Aquatic Biology, Volume 5, pages 41 – 48.
Findlay HS, Kendall MA, Spicer JI & Widdicombe S. 2009. Future high CO2 in the intertidal may compromise adult barnacle Semibalanus balanoides survival and embryonic development rates. Marine Ecology – Progress Series, Volume 389, pages 193 – 202.
Smirthwaite JJ, Rundle SD & Spicer JI. 2009. The use of developmental sequences for assessing evolutionary change in gastropods. American Malacological Bulletin, Volume 27, pages 105 – 111.
Smirthwaite J, Rundle SD, Bininda-Emonds ORP & Spicer JI. 2007. An integrative approach identifies sequence heterochronies in pulmonate snails. Evolution and Development, Volume 9, pages 122 - 130.
Spicer JI & Rundle SD. 2007. Plasticity in the timing of physiological development: Physiological heterokairy - what is it, how frequent is it, and does it matter? Comparative Biochemistry and Physiology, Part A., Volume 148, pages 712 - 719.
Spicer JI. 2006. Gut-reaction by heartless shrimps: Experimental evidence for the role of the gut in circulation before cardiac ontogeny. Biology Letters, Volume 2, pages 580 - 582.
Spicer JI & Rundle SD. 2006. Out of place and out of time: Towards a more integrative approach to heterochrony. Animal Biology, Volume 57, pages 487 - 502.
Spicer JI & Eriksson SP. 2003. Does the development of respiratory regulation always accompany the transition from pelagic larvae to benthic fossorial postlarvae in the Norway lobster Nephrops norvegicus (L)? Journal of experimental Marine Biology and Ecology, Volume 295, pages 219 - 243.
Spicer JI & J-O Strömberg. 2003. Developmental changes in the responses of O2 uptake and ventilation to acutely declining O2 tensions in larval krill Meganyctiphanes norvegica. Journal of Experimental Marine Biology and Ecology, Volume 295, pages 207 - 218.
Spicer JI. 2001. Development of cardiac function in crustaceans: patterns, processes and implications. American Zoologist, Volume 41, pages 1068 – 1077.
Morritt D & Spicer JI. 1999. Developmental ecophysiology of the beachflea Orchestia gammarellus (Pallas) (Crustacea: Amphipoda). III Physiological competency as a possible explanation for timing of hatchling release. Journal of Experimental Marine Biology and Ecology, Volume 232, pages 275 - 283.
Spicer JI & El-Gamal MM. 1999. Hypoxia accelerates the development of respiratory regulation in brine shrimp - but at a cost. Journal of experimental Biology, Volume 202, pages 3637 - 3646.
Morritt D & JI Spicer. 1996. Culture of embryonic amphipods (Crustacea). Journal of the Marine Biological Association of the United Kingdom, Volume 76, pages 361 - 376.
Morritt D & Spicer JI. 1996. Developmental ecophysiology of the beachflea Orchestia gammarellus (Pallas) (Crustacea: Amphipoda). I Female control of brood pouch Journal of Experimental Marine Biology and Ecology, Volume 207, pages 191 - 203.
Morritt D & Spicer JI. 1996. Developmental ecophysiology of the beachflea Orchestia gammarellus (Pallas) (Crustacea: Amphipoda) II Embryonic osmoregulation Journal of Experimental Marine Biology and Ecology, Volume 207, pages 191 - 203.
Spicer JI & Morritt D. 1996. Ontogenic changes in cardiac function in crustaceans, Comparative Biochemistry and Physiology, Part A, Volume 114, pages 81 - 89.
Morritt D & Spicer JI. 1995. Changes in the pattern of osmoregulation in the brackish water amphipod Gammarus duebeni (Crustacea) during embryonic development. Journal of Experimental Zoology, Volume 273, pages 271 - 281.
Spicer JI. 1995. Ontogeny of respiratory function in crustaceans exhibiting either direct or indirect development. Journal of Experimental Zoology, Volume 272, pages 413 - 418.
Spicer JI. 1995. Effect of water-borne copper on respiratory and cardiac function during the early ontogeny of the brine shrimp Artemia franciscana Kellogg 1908 (Branchiopoda: Anostraca). Journal of Comparative Physiology, Volume 165B, pages 490 - 496.
Spicer JI. 1994. Ontogeny of cardiac function in the brine shrimp Artemia franciscana Kellogg 1906 (Branchiopoda: Anostraca), Journal of Experimental Zoology, Volume 270, pages 508 - 516.
Books and Chapters
Nancollas SJ, & Spicer JI. 2024 Emersion and Hypoxia. Book Chapter In: ecophysiology of the European Green Crab (Carcinus maenas) and Related Species. Academic Press, Cambridge, US, 207-229.
Spicer JI. Biodiversity: A Beginner's Guide (revised and updated edition). Oneworld Publications, London (2021).
Spicer JI, Tills O, Truebano M, Rundle SD. 2018. Developmental Plasticity and Heterokairy. Book Chapter In: Development and Environment, Springer, Switzerland. Eds: Burggren W, Dubansky B.
Spicer, J.I. Physiological heterochrony. In (eds Warburton, S., W.W. Burggren, B. Pelster, C.L. Reiber and J.I. Spicer) Comparative Developmental Physiology. Contributions, tools and trends. Oxford University Press Inc., New York (2006).
Warburton S, Burggren WW, Pelster B, Reiber CL & Spicer JI. 2006. (editors) Comparative Developmental Physiology. Contributions, tools and trends. Oxford University Press Inc, New York (2006).
Software
Hardware and software for visualising, quantifying and studying developing embryos: https://github.com/otills/embryophenomics
Patents
Tills O, Rundle SD, Culverhouse P, Spicer JI & Bitterli TS. 2011. Method and system for determining characteristics of an embryo and uses thereof. Patent, World Intellectual Property Organization.