Habitat fragmentation and evolution of dispersal. Jean-François Le Galliard CNRS, University of Paris 6, France
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1 Habitat fragmentation and evolution of dispersal Jean-François Le Galliard CNRS, University of Paris 6, France
2 Habitat fragmentation : facts Habitat fragmentation describes a state (or a process) of discontinuities (fragments) within the preferred living area (habitat) of a species. The classical paradigm of population ecology is that of a single, large and homogeneous population, but it is widely recognised that most populations are fragmented and heterogeneous -> implications for ecological and evolutionary processes?
3 Habitat destruction vs. habitat fragmentation Habitat destruction is associated with massive habitat loss, fragmentation and habitat degradation ~ 83 % land surface affected by human activities Forest fragmentation (green area) in Finland from 1752 to 1990 Habitat destruction includes several processes: Reduction in the total area of the habitat Increase in number of habitat patches Decrease in habitat patches area Increase in isolation of habitat fragments Possibly, a decrease in habitat quality Fahrig. Ann. Rev. Ecol. Syst
4 Effects of habitat destruction on biodiversity Habitat destruction is considered as one of the main cause of species loss on earth with overexploitation and species invasion according to the 2006 IUCN statistics 16,119 species are threatened with extinction in the Red List. 99% of threatened species are at risk from human activities. Humans are the main cause of extinction and the principle threat to species at risk of extinction. Habitat loss and degradation are the leading threats. They affect 86% of all threatened birds, 86% of the threatened mammals assessed and 88% of the threatened amphibians. Examples of species threatened by habitat loss in Europe (21 listed endangered) Erismature à tête blanche Grenouille des Pyrénées Silene diclinis
5 Ecological consequences of habitat fragmentation
6 Ecology of fragmented habitats Spatial structure : existence of discrete, localised patches of preferred habitat separated by a matrix of non-preferred habitat patchy distribution spatial organisation : number and spatial distribution of patches Local demography : small patches are more likely to go extinct and more variable than large populations Connectivity : patches are separated by a matrix of non-preferred habitat putting limits on dispersal abilities connectivity : number, size and spatial distribution of corridors permeability : matrix quality and spatial structure
7 A case example Habitat fragmentation Granville fritillary butterfly (Finland) Hanski. Nature
8 Models of habitat fragmentation The Levin s model (occupancy model) m p occupied empty e p = m p (1 p) e p Very fast local dynamics p* = 0 p* = (m-e)/m The population is in a balance between migration and extinction There is a threshold migration rate for population viability (m = e) below the threshold, the population is viable above the threshold, the population goes extinct Levins. Bull. Ent. Soc. Entom. USA
9 Models of habitat fragmentation The source-sink model (Pulliam) Productive habitats Non-productive habitats Source : net exporter of migrants (high productivity) Sink : net importer of migrants (low productivity) The simple source sink-models predict that Absolute sinks would not persist in the absence of sources A large proportion of a population can exist in sink habitats In the case of density-dependent regulation Sinks are set above their carrying capacity Sources are set below their carrying capacity Asymmetric migration between habitat patches (unbalanced dispersal) Pulliam. Am. Nat
10 Models of habitat fragmentation The metapopulation model discrete spatial structure two spatial scales (local and regional) local persistence for at least a few generations dominant effects of extinction-colonisation dynamics Hanski s metapopulation model : incidence functions «occupancy» models designed for butterflies populations extinction rate depends on patch area colonisation rate depends on size of and distance to neighbouring patches State variable : occupancy of a given patch i Model parameters and incidence functions E = min[e/a x,1] extinction rate decreases with patch area C = β exp(-α d ij ) p j A j colonisation rate decreases with distance and increases with patch crowding and patch areas Hanski. Metapopulation ecology
11 Rescue effect and alternative equilibria Very low metapopulation occupancy = negative metapopulation growth rate due to low colonisation rate Higher occupancy = higher colonisation rate (rescue effect) favors increased growth rate Very high occupancy = crowding and population regulation at the regional level Predicted (theory) Observed (66 networks) Predicted (empirical model) Hanski. Nature
12 Contrasted effects of habitat destruction No community scale response due to a large variation in species-specific responses 3 common small mammals (from large to small) snakes Robinson et al. Science Clonal / Non-clonal plants
13 Habitat destruction and species decline Large-scale experimental habitat destruction experiment in Brasil (13 years, 23 patches) 12 pristine forest patches 11 isolated patches from 10 to 600 ha Monitoring of the bird community and analysis with a statistical model of patch turnover in species presence/absence Extinction rate according to the «best» statistical model Positive effect of fragmentation on extinction rates, but results are highly variable and many species are insensitive to habitat fragmentation Negative effect of patch size on extinction rate Ferraz et al.. Science
14 Diverse effects of habitat fragmentation: why? Details that can matter Landscape structure : corridors and matrices, spatial scale Behavioural flexibility : context-dependent dispersal Community processes : species interactions (eg competition-colonisation trade-off, complementarities ) Example: density-dependent dispersal Constant dispersal = can cause rescue at low population density and synchronises local population dynamics Negative density-dependent = precipitates population extinction and limits spatial synchronisation Example in root voles (Microtus oeconomus) from Norway. Negative density-dependent dispersal is common in vertebrates. Andreassen et al. Proc. Roy. Soc
15 Evolutionary consequences of habitat fragmentation
16 Levels of selection in fragmented populations Selection within demes (intrademic selection) social interactions kinship structures Selection between demes (interdemic selection) dispersal and colonisation migration and founder effects «Metapopulation effect» Olivieri and Gouyon Examples of antagonistic selective pressures Cooperative behaviour in mammals = selected for between demes but counterselected within each deme Dispersal in plants = counterselected within the deme but selected between demes Virulence in parasites = selected for within the deme but can be selected against between demes Habitat fragmentation causes selection due Genetic heterogeneity : inbreeding and kinship structure. Demographic heterogeneity : e.g. density-dependence. Environmental heterogeneity : e.g. habitat quality.
17 Evolution of dispersal rate : kin selection Basic assumptions homogeneity in deme sizes homogeneity in deme structures kin selection due to genetic heterogeneity Interactions with Philopatry Dispersal Relatives Many Few Conspecifics Some Some Kin competition Dispersal Hamilton & May Nature Kin cooperation Philopatry Perrin & Goudet. Oxf Univ Press 2001
18 Evolution of dispersal rate : demographic heterogeneity Basic assumptions no kinship structure variance in patch occupancy due to local extinction selection due to demographic heterogeneity (avoidance of competition) Model of successional dynamics and plant dispersal More colonisation opportunities Fast succession Less local competition Slow succession Ronce et al. Am Nat
19 Evolution of dispersal rate : environnemental heterogeneity Basic assumptions : habitat heterogeneity selection due to environmental heterogeneity two traits : dispersal and local adaptation traits Habitat variation alone two habitats - no kin selection local maladaptation = cost of dispersal = loss of migration local adaptation = benefits of specialisation = evolution of specialist strategies Two non-dispersive specialist strategies Habitat + temporal variation - no kin selection temporal variation = risk spreading benefits = evolution of partial migration coevolution of local adaptation can lead to various patterns of existence and coexistence between the two non-dispersive specialists and a generalist disperse strategy Kisdi. Am Nat
20 Evolution of social structures Low High Individual mobility Low Territorial solitarily breeding species Dispersed solitarily breeding species High Territorial cooperatively breeding species Solitary slime molds Reproductive altruism Slime molds fruiting body After Crespi and Choe Camb. Univ. Press 1997 Sherman et al. Behav. Ecol. 1995
21 Life history evolution: empirical facts
22 Mother-offspring competition and natal dispersal Manipulation of mother presence in experimental patches of natural habitat Common lizard : assessment of natal dispersal during two successive years Le Galliard et al. Proc. Roy. Soc. 2003
23 Mother-offspring competition and natal dispersal Manipulation of mother presence in experimental patches of natural habitat Root voles: assessment of natal dispersal during 20 days 1.0 A) Natal dispersal probability Females in control plots Females in treatment plots Males in control plots Males in treatment plots Overlap with the adult female B) Le Galliard et al. Behav. Ecol. In review
24 Evolution of plant dispersal on islands «Mainland» «Island» Comparative analysis of dispersal abilities for two plant species based on morphological measurements The loss of migration abilities is a common evolutionary syndrome of island species / populations Cody and Overton. J. Ecol. 1996
25 Evolution of flight behaviour in butterflies «Woodland» butterflies «Agricultural» butterflies Raised in a common garden and investigated for their flight behaviour in the laboratory Pararge aegeria Merckx et al. Proc. Roy. Soc. London 2003
26 Dispersal behaviour and landscape structure in spiders Isolated Connected Continuous Raised in a common garden and investigated for the «tip-toe» behaviour in the laboratory Passive dispersal seems to be selected against in more fragmented habitats! This can be explained by dominant effects of the cost of dispersal or specialisation Bonte et al. Anim. Behav. 2006
27 Dispersal and habitat specialisation in different spider species Intensity of «tip-toe» behaviour indicates passive dispersal ability Dispersive species are habitat generalists -> dispersal may be counterselected in isolated landscapes due to habitat specialisation Index of habitat specialisation based on local recordings and literature review in Europe Bonte et al. Proc. Roy. Soc. Lond. 2003
28 Key references Colas B. et al Adaptive responses to landscape disturbances: empirical evidence. Pp in Evolutionary Conservation Biology (eds. Ferrière et al.). Cambridge University Press. Fahrig, L Effects of habitat fragmentation on biodiversity. Annual Review of Ecology and Systematics. 34: Ferraz, G. et al A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. Science 315: Le Galliard, J.-F., Ferrière, R. and J. Clobert Mother-offspring interactions affect natal dispersal in a lizard. Proceedings Royal Society London B 270: Hanski I Metapopulation dynamics. Nature 396: Hanski I Metapopulation ecology. Oxford University Press. Ronce and Olivieri Life history evolution in metapopulations. Pp in Ecology, Genetics and Evolution of Metapopulations (eds. Hanski and Gagiotti). Elsevier.
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