Ecological effects of climate warming on populations Jean-François Le Galliard CNRS – iEES Paris CNRS/Ens – CEREEP/Ecotron IleDeFrance
Global warming and climate changes
Warming in the context of global changes
+ effects of habitat destruction and alteration
Smith et al. Ecology. 2009
Extant and speed of global warming
IPCC report. 2007.
Extant and speed of global warming
IPCC report. 2007.
Spatial distribution of climate warming Climate warming during the last 30 years according to observations
Walther et al. Ecological responses to recent climate change. Nature 2002, 416, 389-395.
Concurrent changes in rainfall patterns Changes in annual rainfall during the last 30 years according to observations
Walther et al. Ecological responses to recent climate change. Nature 2002, 416, 389-395.
Examples of climate data
Données et figures Météo France (www.meteo.fr/ )
Examples of climate data in long-term study sites
Mont Lozère, Lozère (1450 m) Sites de suivi du lézard vivipare (M. Massot & J. Clobert) Augmentation de l’ordre de +2°C pendant 30 ans Données Météo-France Lozère Mont Aigoual & Mas de la Barque
Mont Serein, Vaucluse (1420 m) Site de suivi de la vipère d’Orsini (J.-P. Baron) Augmentation de l’ordre de +3°C pendant 30 ans Données Météo-France Vaucluse Carpentras & Mont Serein
Scenarios for the future: temporal trends
+ 0.6 °C mean change during last century
+ 1.5 à 4.5 °C mean expected change during next 50 years
Concurrent changes in rainfall, greenhouse gas concentrations, or water acidity but with strong regional and seasonal contrasts IPCC (2007) Climate Change 2007: Synthesis Report. Summary for Policymakers (eds R. K. Pachauri & A. Reisinger).
Scenarios for the future: spatial variability Projected surface temperatures for the next century
IPCC (2007) Climate Change 2007: Synthesis Report. Summary for Policymakers (eds R. K. Pachauri & A. Reisinger).
Effects of climate warming on living organisms
Thermal effects in ecological systems Temperature increase due to global warming Individual physiology Physiology of conspecifics Habitat structure and quality Physiology of heterospecifics Interspecific relationships Dispersal responses (habitat tracking) Functional traits (e.g., photosynthesisrespiration-C sequestration)
Life history strategy Population growth and dynamics Species range and distribution Community structure Ecosystem processes
Thermal effects on physiology and organisms Thermal effects on • speed of “simple” chemical reactions • speed of complex reactions chains (e.g., >104 proteins and 105 reactions in vertebrate cells) • speed of organism’ wide processes such as ingestion, digestion, excretion, etc = whole-organism energetic and performances Arrhenius rule (1884) n×A+m×B→C+D r = k(T) × [A]n’ × [B]m’ k(T) = k0 × e-Ea/(R ×T) where Ea is activation energy and R is gaz constant
Example of thermal effects on whole-organism locomotor and feeding performances
van Damme, R., Bauwens, D. & Verheyen, R. F. (1991) The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard Lacerta vivipara. Functional Ecology, 5, 507-517.
Example of thermal effects on metabolic rates
Streicher, J. W., Cox, C. L. & Birchard, G. F. (2012) Non-linear scaling of oxygen consumption and heart rate in a very large cockroach species (Gromphadorhina portentosa): correlated changes with body size and temperature. pp. 1137-1143.
From physiology to ecology: coupled energy and mass balance (energy and water budget) Heat energy balance equation
Mass balance equation
Water balance
Kearney, M. & Porter, W. (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. Ecology Letters, 12, 334-350.
From physiology to ecology: energy budget and life history trajectories in animals
Kordas, R. L., Harley, C. D. G. & O'Connor, M. I. (2011) Journal of Experimental Marine Biology and Ecology, 400, 218-226.
From physiology to ecology: effects of warming on spatial distribution of western fence lizards
Buckley, L. B. (2008) Linking traits to energetics and population dynamics to predict lizard ranges in changing environments. The American Naturalist, 171, E1-E19.
Global effects on metabolic rates in terrestrial ectotherms a. Change in temperature in the environment b. Absolute change in metabolic rate due to metabolism-temperature dependency c. Relative change
Dillon, M. E., Wang, G. & Huey, R. B. (2010) Global metabolic impacts of recent climate warming. Nature, 467, 704-U88.
Global effects on metabolic rates in terrestrial ectotherms
Dillon, M. E., Wang, G. & Huey, R. B. (2010) Global metabolic impacts of recent climate warming. Nature, 467, 704-U88.
Thermal adaptation: performance curves
Huey, R. B. & Kingsolver, J. G. (1989) Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology and Evolution, 4, 131-135. Kingsolver, J. G. (2009) The Well-Temperatured Biologist. American Naturalist, 174, 755-768.
Thermal adaptation: performance curves Locomotor performances in laboratory crickets raised at different temperatures
Growth performances of hot springs cyanobacteria Synechococcus
Thermal gradient Lachenicht, M. W., Clusella-Trullas, S., Boardman, L., Le Roux, C. & Terblanche, J. S. (2010) Effects of acclimation temperature on thermal tolerance, locomotion performance and respiratory metabolism in Acheta domesticus L. (Orthoptera: Gryllidae). Journal of Insect Physiology, 56, 822-830. Kingsolver, J. G. (2009) The Well-Temperatured Biologist. American Naturalist, 174, 755-768.
From performance curves to population and ranges Thermal dependence of growth: increase in metabolism vs drop in aerobic scope
Blood flow measured by NMR: optimisation at Topt
Mismatch between oxygen supply and demand: accumulation of succinate in liver
Demographic collapse with extreme summer temperatures
Pörtner, H. O. & Knust, R. (2007) Climate Change Affects Marine Fishes Through the Oxygen Limitation of Thermal Tolerance. pp. 95-97.
Complex thermal effects in ecological systems Temperature increase due to global warming Individual physiology Physiology of conspecifics Habitat structure and quality Physiology of heterospecifics Interspecific relationships Dispersal responses (habitat tracking) Functional traits (e.g., photosynthesisrespiration-C sequestration)
Life history strategy Population growth and dynamics Species range and distribution Community structure Ecosystem processes
Effects of habitat loss on polar bears
Effects of ice free periods on annual survival of adult females (as well as breeding rates and cub litter survival) – based on five years of field data (2001-2005) with marked animals
Regehr, E. V., Hunter, C. M., Caswell, H., Amstrup, S. C. & Stirling, I. (2010) Survival and breeding of polar bears in the southern Beaufort Sea in relation to sea ice. Journal of Animal Ecology, 79, 117-127.
Warming effects on habitat and species loss Observed and predicted species loss (extinction per million species per year)
Predicted extinction rates from models of climate and habitat changes • habitat loss • species-area curves
Observed, current extinction rates according to IUCN red lists
Leadley, P., H. M. Pereira, R. Alkemade, J. F. Fernandez-Manjarrés, V. Proença, J. P. W. Scharlemann, and M. J. Walpole. 2010. Biodiversity Scenarios: Projections of 21st century change in biodiversity and associated ecosystem services, Pages 132, Technical Series Montreal, Secretariat of the Convention on Biological Diversity.
Predictions from climate-envelope models Calculation of climate envelopes in 1,103 animal and plant species Projection of climate envelopes in the future based on climate scenarios and two modes of dispersal Calculation of extinction rates based on speciesarea curves S = cAz Global extinction risks should increase by 15-37 % by 2050 with large variation across biomes
Similar predictions in other taxa and with other methods + increased extinction risks due to habitat destruction Thomas et al. (2004) Extinction risks from climate change. Nature, 427, 145-148. Thuiller, W., Lavorel, S., Araujo, M. B., Sykes, M. T. & Prentice, I. C. (2005) Climate change threats to plant diversity in Europe. Proceedings of the National Academy of Sciences of the United States of America, 102, 8245-8250.
Example of extinction driven by climate changes Loss of two amphibian species from cloud forests in Costa Rica (no observation since 15 years) Concurrent with climate change in the area (dryness) and emergence of disease
Pounds, J. A., Fogden, M. P. L. & Campbell, J. H. (1999) Biological response to climate change on a tropical mountain. Nature, 398, 611-615.
Complex thermal effects in ecological systems Temperature increase due to global warming Individual physiology Physiology of conspecifics Habitat structure and quality Physiology of heterospecifics Interspecific relationships Dispersal responses (habitat tracking) Functional traits (e.g., photosynthesisrespiration-C sequestration)
Life history strategy Population growth and dynamics Species range and distribution Community structure Ecosystem processes
Climate effects on trophic interactions: example Correlation with fledging success
Fluctuations in NAO (winter climate) r2 = 0.11
Surface temperature at sea r2 = 0.47
Abundance of preys (herrings) r2 = 0.53
Size of captured preys r2 = 0.70 Durant, J. M., Anker-Nilssen, T. & Stenseth, N. C. (2003) Trophic interactions under climate fluctuations: the Atlantic puffin as an example. Ecol. Lett. pp. 1461-1466.
Climate effects on trophic interactions: example
Best multivariate model
Durant, J. M., Anker-Nilssen, T. & Stenseth, N. C. (2003) Trophic interactions under climate fluctuations: the Atlantic puffin as an example. Ecol. Lett. pp. 1461-1466.
Direct and indirect effects on trophic interactions
Net effect on the prey population Kordas, R. L., Harley, C. D. G. & O'Connor, M. I. (2011) Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. Journal of Experimental Marine Biology and Ecology, 400, 218-226.
Complex thermal effects in ecological systems Temperature increase due to global warming Individual physiology Physiology of conspecifics Habitat structure and quality Physiology of heterospecifics Trophic relationships Dispersal responses (habitat tracking) Functional traits (e.g., photosynthesisrespiration-C sequestration)
Life history strategy Population growth and dynamics Species range and distribution Community structure Ecosystem processes
Example 1 : highly mobile species can respond very quickly to climate warming Sachem skipper (Atalopedes campestris): widespread and good dispersing butterfly
The overwintering range of this species (shaded area) has expanded quickly northward (lighter shading) during the past 40 years and has tracked remarkably well the shifting thermal isocline of the January average minimum -4°C isotherm, which is lethal in this species Crozier, L. (2003) Oecologia, 135, 648-656
Example 2: some species could be trapped in an evolutionary state of low mobility Knapweed (Centaurea corymbosa): rare plant endemic of cliffs in southern France
This species is a very poor disperser (data represent distribution of seed dispersal distances from the maternal plant), which we predict will be unable to track changing climates
Colas, B., Olivieri, I. and Riba, M. (1997) Proceedings of the National Academy of Sciences of the United States of America, 94, 3471-3476
Lessons from the past: Quaternary range shifts Range expansion of oak trees (Quercus spp.) northward during the late glacial and Holocene period obtained from pollen record in Europe
Brewer, S., Cheddadi, R., de Beaulieu, J.L. & Reille, M. (2002) Forest Ecology and Management, 156, 27-48.
Lessons from the past: Quaternary range shifts Range expansion of oak trees (Quercus spp.) during the Holocene period in the UK Diffusion model with a Gaussian dispersal kernel and DID growth
Birks, H. J. B. (1989) Journal of Biogeography, 16, 503-540 Clark, J.S. (1998) American Naturalist, 152, 204-224.
Lessons from the past: Quaternary range shifts are numerous but not so simple … Contrasted responses of tree (Picea and Quercus) to Quaternary climate change
Epicea
Chêne
Davis, M.B. & Shaw, R.G. (2001). Science, 292, 673-679.
Lessons from the present: species often respond by shifting their latitudinal or altitudinal range
Parmesan, C., and G. Yohe. 2003. Nature 421:37-42.
Yet, species differ in their ability to respond to climate change through range shifts
Range shifts in butterflies
Northward range shift
Northward shifts in thermoclines
Seasonal sums of daily mean temperatures above 5°C in Finland
Pöyry, J., Luoto, M., Heikkinen, R.K., Kuussaari, M. & Saarinen, K. (2009) Global Change Biology, 15, 732-743.
Species differ in their ability to respond to climate change through range shifts Multivariate regression corrected for phylogenetic relatedness among species ca. 12 % variation
Positive effect of species mobility score
ca. 10 % variation
Forest edge species have shifted more
Predictions of climate niche models may not fit observed range shifts Example of the range shift in Finland of the map butterfly Observed range shift
Predicted range shift from a Europe-wide climate niche model
Black pixel = presence Red pixel = absence White pixel = not enough reliable data
Mitikka, V., Heikkinen, R.K., Luoto, M., Araujo, M.B., Saarinen, K., Poyry, J. & Fronzek, S. (2008). Biodiversity and Conservation, 17, 623-641.
Digression: the niche concept in ecology
Climate change, ecology and the niche concept Our investigation of climate change effects on populations has led us to consider multiple pathways by which climate warming could influence single species • through the physiological performances of single organisms, which are dictated by boundaries conditions such as critical thermal limits and thermal optima • through the interactions with other species such as preys and predators, which determines coexistence and stability of complex ecological networks where the species is involves •through the spatial distribution of climate conditions, which dictates the suitability of the thermal landscape for species persistence These multiple pathways are all related to the historical concept of the ecological niche broadly defined as the “habitat and role of a species in the ecosystem”
Various niche definitions Grinnellian niche concept (1907-1924) The niche of a species is determined by the habitat where it lives and the associated adaptations. Sometimes called the “habitat niche”. Eltonian niche concept (1927) The niche of a species describes the place of the species in a community (e.g. trophic networks) including its relations to food and enemies and to some extent to other factors. Sometimes called the “functional niche”. Hutchinsonian niche concept (1957) The niche is a property of a species and not of its environment. It is described in a space of environmental variables including biotic and abiotic factors that represent the limit of species persistence. Two similar species according to their niche cannot coexist (competitive exclusion).
Hutchinsonian niche concept Fundamental niche The combinations of environmental conditions that permit species persistence in the absence of competitive exclusion (or biotic interactions) Realized niche The actual region occupied by the species given biotic interactions
Example of resource utilization functions
Begon M, Harper JL, Towsend CR, 1996. Ecology. Individuals, populations and community, 3 ed: Blackwell Science.
Niche quantification and global warming Experimental niche models Based on an analysis of species persistence across manipulated range of environmental conditions or across transplant experiments. Allows to quantify the fundamental niche directly experimentally. Rarely used in global warming studies. Mechanistic niche models A calculation of the species niche from physiological and performance data. Allow to quantify the fundamental niche indirectly from lower-level organismal traits. More frequently used in global warming studies. Statistical niche models (or ecological niche models). An analysis of the spatial distribution of the species and a statistical model of occurrence data. Allows to calculate the realized niche empirically. Frequently used in global warming studies.
Major ecological responses in single species
Four major ecological responses in single species Temperature increase due to global warming Shifts in phenology (timing of key annual and seasonal events) Changes in activity patterns Altitudinal range shifts Latitudinal range shifts Change in body size-body mass (temperature-size rule)
Observed changes in phenology Spring activity in temperate climates (Europe and North America, >1960) • earlier arrival dates from migratory bird species • earlier winter emergence of butterflies • earlier breeding dates of birds • earlier mating and breeding dates of amphibians • early sprouting of trees and flowering of plants Advancement of spring activities more pronounced in “precocial” species
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J.-M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature, 416, 389-395. Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology and Systematics, 37, 637-669. Root, T. L., Price, J. T., Hall, K. R., Schneider, S. H., Rosenzweig, C. & Pounds, J. A. (2003) Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60.
Observed changes : grape harvest dates
Chuine, I., Yiou, P., Viovy, N., Seguin, B., Daux, V. & Ladurie, E. L. (2004) Historical phenology: Grape ripening as a past climate indicator. Nature, 432, 289-290.
Observed changes : multivotinism in insetcs Advancement and extension of activity season in insects
Increased number of generations per year (voltinism)
Test in 263 butterfly and moth species from Central Europe a multivotine life cycle
Altermatt, F. (2010) Climatic warming increases voltinism in European butterflies and moths. Proceedings of the Royal Society of London Series B-Biological Sciences, 277, 1281-1287.
Observed changes : breeding dates in a passerine Compilation of 25 long-term studies Analysis of the annual trend for laying dates and spring temperatures
Both et al. (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proceedings of the Royal Society B-Biological Sciences, 271, 1657-1662.
Observed changes : return dates of migration Bird migration patterns (Scandinavia) • earlier arrival dates in 23 bird species at North Sea • relationship with North Atlantic Oscillation (winter climate) over 40 years • 2 to 20 days advancement depending on species • effects more pronounced in long-distance migratory species Skid populations (Channel) • earlier arrival dates of skid populations in the Channel • relationship with North Atlantic Oscillation (winter climate) and sea temperature over 20 years • up to 120-150 days advancement during climate extremes • causes strong difficulties for fisheries Phenological changes can have direct effects on fitness (e.g. activity budget) and indirect effects via interactions with other species (e.g. preys)
Consequences of shifts in phenology
Laying date
Example of selection for temporal matching
Spring temperature
Nussey, D. H., Postma, E., Gienapp, P. & Visser, M. E. (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science, 310, 304-306.
Four major ecological responses on single species Temperature increase due to global warming Shifts in phenology (timing of key annual and seasonal events) Changes in activity patterns Altitudinal range shifts Latitudinal range shifts See before Change in body size-body mass (temperature-size rule)
Four major ecological responses on single species Temperature increase due to global warming Shifts in phenology (timing of key annual and seasonal events) Changes in activity patterns Altitudinal range shifts Latitudinal range shifts Change in body size-body mass (temperature-size rule)
Examples of effects in vertebrates Some contrasted warming effects on body size • lower body size at birth in red deer from Norway with persistent effects until adulthood (Post et al. Proc London 1997) • higher body size in freshwater fish species from high-altitude lakes (Krajick Science 2004) • larger body size in yearlings and adult common lizards due to changes in phenology (Chamaillé-James et a. GCB 2006, Le Galliard et al. J Anim Ecol 2010)
Review of all published studies • a general tendency for smaller body size in response to warming in aquatic organisms (Daufresne et al. PNAS 2009) = temperature-size rule (well described in ectotherms) • … but some variation exists around this rule (Gardner et al. TREE 2011) = complex determination of body size
Temperature-size rule: size at age shift bacteria
phytoplancton
fish species
marine fish species Daufresne, M., Lengfellner, K. & Sommer, U. (2009) Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106, 12788-12793.
Analysis of body size trends in birds Contrasted evidences from museum specimens of 8 species of passerine birds from south-eastern Australia along a latitudinal gradient < 1950
> 1950
Gardner, J. L., Heinsohn, R. & Joseph, L. (2009) Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines. Proceedings of the Royal Society B-Biological Sciences, 276, 3845-3852.
Evolutionary changes in response to warming
Climate changes should influence the spatial range A. Large species ranges g min war cool margin
optimal thermal regime
war
war
shift contraction
g min
g min
warm margin
no dispersal
with dispersal
B. Small species ranges expansion
g min war cool margin
optimal thermal regime
g min war
war
g min
extinction
extinction
no dispersal
with dispersal
warm margin
Le Galliard, Massot & Clobert (2012). In press.
Dispersal behavior is key to the ecological responses to climate changes Climate change (warming, drying, etc)
Spatial shift in climate niche of the species
Dispersal response
Adaptive response
Phenotypic plasticity
Genetic adaptation
The pace of climate change: strong selection! +1°C change = 100-150 km latitudinal shift Current change = 0.08 to 1.26 km/year
Evolution of thermal tolerance: genetic evidences Latitudinal clines in gene frequency in Drosophila melanogaster (sampling of 4 genetic markers in Eastern Australia) Warm-cold cline
Adh locus = adaptation to thermal and humidity conditions in the laboratory and in natural populations
Ln(3R)Payne = chromosomal inversion on another chromosome than Adh
Umina, P. A., Weeks, A. R., Kearney, M. R., McKechnie, S. W. & Hoffmann, A. A. (2005) A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science, 308, 691-693.
Evolution of dispersal in wing dimorphic insects
Simmons, A. D. & Thomas, C. D. (2004) Changes in dispersal during species' range expansions. American Naturalist, 164, 378-395. Thomas, C. D., Bodsworth, E. J., Wilson, R. J., Simmons, A. D., Davies, Z. G., Musche, M. & Conradt, L. (2001) Ecological and evolutionary processes at expanding range margins. Nature, 411, 577-581.
