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The Environment Institute
                    Where ideas grow




   Dr Melanie Lancaster
   Pines and paddocks: Socioecology and population
   genetics of marsupials in fragmented systems
Pines and paddocks: Socio-ecology and
   population genetics of marsupials
in fragmented south-eastern Australia

                  Melanie Lancaster
             Earth and Environmental Sciences
                 The University of Adelaide

     Steven J.B. Cooper, Susan Carthew, Andrea C. Taylor
Molecular Ecology
        INDIVIDUAL            POPULATION                SPECIES


      Use of genetic tools to answer ecologically important
                              questions

Identification of individuals to a source population

Population processes: migration, dispersal (ie. juvenile, sex-biased), GENE
  FLOW

Social structure: Mating systems, site fidelity, mate fidelity

Predict species responses to environmental changes, human impacts, etc.
Background (mine)
                       PhD research
• Small population of fur seals on Macquarie Island
• Suspected interbreeding among three species
   – Different recolonisation histories
• Tissue samples collected from entire pup cohorts between
  1992 and 2003



• Extensive observational data – territory locations,
  pupping sites
• Species composition of the population
• Hybrids?
• Costs of hybridisation?
PhD research – species identification
                                                Genetic screening of individuals =>
         70                                    identification to a source species or
                                                            hybrid class
         60

         50
% PUPS




         40

         30

         20

         10

          0
          1992   1994   1996     1998   2000   2002

                          YEAR
                                                                   Lancaster et al. (2006)
                                                                   Molecular Ecology
PhD research – mating systems




      Genetic analysis of paternity =>
         identify fitness cost to
               hybridisation




Lancaster et al. (2007)
Molecular Ecology
Molecular Ecology
          INDIVIDUAL              POPULATION                     SPECIES

    Use of genetic tools to answer ecologically important
                            questions

Identification of individuals to a source population

Population processes: migration, dispersal (ie. juvenile, sex-biased), GENE FLOW

Social structure: Mating systems, site fidelity, mate fidelity


    Predict species responses to environmental changes, human
                             impacts, etc.
Forest Fragmentation
         • Deforestation as old as the human
         occupation of the earth (Williams 2003)

         • Process has affected more of the earth’s
         surface

         Laurance and Beirregaard 1997:

         • Preserve what we have
         • Plan the future landscape
         • Manage what is left


         Species ecology
         Multi-species approaches
Fragmentation in Australia




  Source: http://adl.brs.gov.au/anrdl/metadata/overviews/alccdr9ab__004/alccdr9ab__00411a10b.pdf
SA - the Lower South-East
           Pre-European Settlement
           • Flora diverse
           • E. baxteri and E. viminalis forests
           and woodlands dominated

           Post-Settlement
           • Large areas cleared after WWII for softwood
           and agricultural land
           • 13 % native vegetation remains
           • Vegetation community composition changed
           • Remaining veg adapted to poor soils and
           poor drainage, incomplete representation
           • Remnants surrounded by cropland, pastures,
           pines


           • Habitats that once supported native fauna
           may no longer be present
Study site
The “Greater Green Triangle” region…when green is bad

• Largest wood fibre producing region in Australia
• Dry, sclerophyll forests isolated by pine stands of various ages
Mammal species

Arboreal and terrestrial
   Sugar gliders, yellow-bellied gliders, Common brushtail and
     ringtail possums, microbats

   Native rats, mice, southern brown bandicoot, yellow-footed
     Antechinus, wallabies (swamp, red-necked), kangaroos,
     wombats, echidnas
Consequences of fragmentation
Populations may become isolated if:
•   Distances between fragments too great to traverse
•   Surrounding habitat too difficult to move through, acts as a barrier to
    dispersal

Individuals within populations do not move out of patch
• Populations become isolated over time and genetically differentiated
from each other
• Within patches, results in increased relatedness, inbreeding, loss of
genetic diversity   Dispersal = ?gene flow
                       No dispersal = NO gene flow

         To assess the impacts of forest fragmentation on
          population processes in key marsupial species
ARC Linkage
Conservation genetics and socio-ecology of marsupials
   in fragmented populations of south-eastern South
        Australia: towards a regional biodiversity
                    management plan
    A/Prof Sue Carthew, Dr Steve Cooper, Dr Andrea Taylor


                        PARTNERS:



      To assess the impacts of forest fragmentation on
       population processes in key marsupial species
Fragmentation case studies
Factors affecting population connectivity in fragmented
   landscapes:
       •   Age of regrowth forest
       •   Surrounding matrix
       •   Habitat shape, edge effects
       •   Lemurs, bird spp., gorillas, pademelons, bats, reptiles, frogs

Sugar gliders (Mansoureh Malekien)
       • Restricted gene flow among some patches
       • Effects greater in small patches isolated by pine
       • Evidence for inbreeding in one patch from parentage analysis


Yellow-footed antechinus (Amanda McLean)
       • Some evidence of differentiation between populations
       • Higher relatedness among females within patches than in continuous
         forest
Common ringtail possum
• Nocturnal arboreal marsupial
• Broad distribution, abundant in a variety of forest habitats
• Generalist herbivore – leaves, flowers, seeds of eucalypt spp., acacia
spp.
• Can build dreys
• Survives in degraded habitats, found in fragmented landscapes
Study site


                                    10             23

                         11
                                              21
                               18                       30
                                                   10         35
                                         23
                              20                         47
      7
               23
15
                    78
     43   74
Data collection
      Site selection based on:

      • patch size
      • distance to neighbouring patch (0.5-
      >10 km)
      • 3 sites within continuous forest
      (distances between sites comparable)




• 251 possums patches within pine
• 189 possums patches within agriculture
• 48 from 3 continuous forest sites
• Genotyped at 15 microsatellites
• Analysed for genetic diversity and genetic differentiation
1. Genetic Diversity
Have possums in patches retained
   genetic diversity?




                                   •   HH and L sig. Lower allelic
                                       richness and heterozygosity

                                   •   Larger patches levels
                                       comparable to continuous
                                       forest

                                   •   Trend towards lower H and
                                       AR in ag patches

                                   YES for some, NO for others,
                                      not related to patch size
                                      alone
2. Population structure
    Do possums move through the pine?

•    Five distinct clusters identified from 8 populations
     sampled   
•    No sub-structure within continuous forest 

•    HH and L genetically isolated 

•    P a subset of continuous forest 

•    SG, W and HS virtually same cluster membership 




                   Yes, but pine hinders dispersal and gene flow
                   Less dispersal into small, isolated patches
2. Population structure
Do possums move through paddocks
   and roadside vegetation?



  8 distinct genetic clusters
  identified


  Significant pop structure
  and isolation


  Limited evidence of gene
  flow/dispersal
Pop Differentiation
      HH          HS          L           P          REN      SG          W          WD
HH
HS         0.05
L          0.19        0.12
P          0.11        0.03        0.17
REN        0.10        0.03        0.13       0.00
SG         0.08        0.03        0.12       0.03     0.04
W          0.06        0.04        0.14       0.05     0.07        0.04
WD         0.09        0.02        0.13       0.02     0.02        0.03       0.05
                                                                                          BG      G      HC     M      PS     RR     SQ     REN
                                                                              BG
                                                                              G            0.08
                                                                              HC           0.08   0.07
   Population pair-wise FST shows all                                         M            0.06   0.04   0.08
  pops except P and R as significantly                                        PS           0.04   0.08   0.11   0.05
                                                                              RR           0.08   0.11   0.09   0.08   0.09
      different (most p < 0.0001)                                             SQ           0.07   0.05   0.07   0.02   0.06   0.07
                                                                              REN          0.03   0.04   0.06   0.03   0.04   0.05   0.03



                        Patches vs Continuous
                                                R1            R2           R3              No sig difference between R1 and R2
                                  R1                           0.12       <0.0001                         (2.5 km)
                                  R2           0.007                        <0.01          Sig. Differentiation of R3 from other
                                  R3           0.038       0.033                                       patches (3 km)
Dispersal patterns

• Mammalian patterns of dispersal
   – Sex-biased
   – Males disperse as juveniles or young adults
   – Females philopatric


• In fragmented landscapes these patterns may be
  disrupted if movement is inhibited

• Use genetic relatedness to look at patterns
PINE                                                                      PADDOCKS
                                                   P and SG not sig
                                  Males                                                                           Males
    0.600                                                                                 0.300

    0.400                                                                                 0.200
                                                                                          0.100
    0.200                                                                   Mean
                                                                                          0.000
r




    0.000                                                                   U
                                                                                        -0.100
    -0.200                                                                  L
                                                                                        -0.200
    -0.400                                                                                         BG    G    HC      M     PS   RR   SQ
               HH     HS      L          P        SG     W      WD


                                      Females                                                                 Females
       0.800                                                                           0.300
       0.600                                                                           0.200
       0.400
                                                                                       0.100
r




       0.200
                                                                                       0.000
       0.000
                                                                                       -0.100
      -0.200
                                                                                       -0.200
                HH     HS         L          P     SG    W      WD
                                                                                                  BG    G    HC     Patch
                                                                                                                     M      PS   RR   SQ
                                         Patch

                              Continuous Forest                                                   All others sig. higher relatedness than
    0.300
    0.200
                                                                                                  expected by chance
    0.100                                                                          Mean
                                                                                                  Both sexes show this trend
r




    0.000
                                                                                   U
    -0.100
                                                                                   L
    -0.200
               R1 M    R2 M           R3 M        R1 F   R2 F        R3 F                         cf continuous forest neither females or
                                          Patch                                                   males show this pattern
Summary
• Intervening matrices appear to hinder dispersal and gene flow of
  possums
   – Less problematic in larger patches than smaller ones
   – Larger patches have comparable genetic diversity to continuous forest
   – Smaller patches HH and L show signatures of genetic isolation through low
     heterozygosity and lower allelic diversity.


• Findings of lower dispersal in both sexes in fragments important
  implications for social structure and mating system


• Pastoral land has greater impact on ringtail possums
   – Depend on several factors
       •   Patch size
       •   Age of pine
       •   Distance to neighbouring patch
       •   Time since isolation
Recommendations and What next?

    – Modelling – which factors affect connectivity – position/distance/
      size of patch but need to quantify

    – Incorporate landscape features – roadside vegetation, plantations,
      grazed remnant vegetation. Circuitscape (uses algorithms from
      electronic circuit theory to predict patterns of dispersal)

    – Incorporate more species

•  Corridors to join patches on the periphery of landscapes
• Multiple potential sources of immigration important for genetic
  diversity
• Continued conservation of large patches that can
  support viable populations to maintain remaining communities
Acknowledgements

Field volunteers for valuable       Australian Research Council Linkage
assistance with possuming           Grants Scheme, with partners:
                                    • Department for the Environment
                                       and Heritage
Martin Pepper for providing
                                    • Forestry SA
photographs                         • Hancock Victorian Plantations
                                    • Nature Foundation of South
Kathy Saint for assistance             Australia
with microsatellite development     • South Australian Museum
The Environment Institute
                        Where ideas grow




   Next Seminar: 27 November

   Professor Kym Anderson
   Regional implications of climate change for the Australian
   wine industry

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Pines and paddocks: socioecology and population genetics of marsupials in fragmented systems

  • 1. The Environment Institute Where ideas grow Dr Melanie Lancaster Pines and paddocks: Socioecology and population genetics of marsupials in fragmented systems
  • 2. Pines and paddocks: Socio-ecology and population genetics of marsupials in fragmented south-eastern Australia Melanie Lancaster Earth and Environmental Sciences The University of Adelaide Steven J.B. Cooper, Susan Carthew, Andrea C. Taylor
  • 3. Molecular Ecology INDIVIDUAL POPULATION SPECIES Use of genetic tools to answer ecologically important questions Identification of individuals to a source population Population processes: migration, dispersal (ie. juvenile, sex-biased), GENE FLOW Social structure: Mating systems, site fidelity, mate fidelity Predict species responses to environmental changes, human impacts, etc.
  • 4. Background (mine) PhD research • Small population of fur seals on Macquarie Island • Suspected interbreeding among three species – Different recolonisation histories • Tissue samples collected from entire pup cohorts between 1992 and 2003 • Extensive observational data – territory locations, pupping sites • Species composition of the population • Hybrids? • Costs of hybridisation?
  • 5. PhD research – species identification Genetic screening of individuals => 70 identification to a source species or hybrid class 60 50 % PUPS 40 30 20 10 0 1992 1994 1996 1998 2000 2002 YEAR Lancaster et al. (2006) Molecular Ecology
  • 6. PhD research – mating systems Genetic analysis of paternity => identify fitness cost to hybridisation Lancaster et al. (2007) Molecular Ecology
  • 7. Molecular Ecology INDIVIDUAL POPULATION SPECIES Use of genetic tools to answer ecologically important questions Identification of individuals to a source population Population processes: migration, dispersal (ie. juvenile, sex-biased), GENE FLOW Social structure: Mating systems, site fidelity, mate fidelity Predict species responses to environmental changes, human impacts, etc.
  • 8. Forest Fragmentation • Deforestation as old as the human occupation of the earth (Williams 2003) • Process has affected more of the earth’s surface Laurance and Beirregaard 1997: • Preserve what we have • Plan the future landscape • Manage what is left Species ecology Multi-species approaches
  • 9. Fragmentation in Australia Source: http://adl.brs.gov.au/anrdl/metadata/overviews/alccdr9ab__004/alccdr9ab__00411a10b.pdf
  • 10. SA - the Lower South-East Pre-European Settlement • Flora diverse • E. baxteri and E. viminalis forests and woodlands dominated Post-Settlement • Large areas cleared after WWII for softwood and agricultural land • 13 % native vegetation remains • Vegetation community composition changed • Remaining veg adapted to poor soils and poor drainage, incomplete representation • Remnants surrounded by cropland, pastures, pines • Habitats that once supported native fauna may no longer be present
  • 11. Study site The “Greater Green Triangle” region…when green is bad • Largest wood fibre producing region in Australia • Dry, sclerophyll forests isolated by pine stands of various ages
  • 12. Mammal species Arboreal and terrestrial Sugar gliders, yellow-bellied gliders, Common brushtail and ringtail possums, microbats Native rats, mice, southern brown bandicoot, yellow-footed Antechinus, wallabies (swamp, red-necked), kangaroos, wombats, echidnas
  • 13. Consequences of fragmentation Populations may become isolated if: • Distances between fragments too great to traverse • Surrounding habitat too difficult to move through, acts as a barrier to dispersal Individuals within populations do not move out of patch • Populations become isolated over time and genetically differentiated from each other • Within patches, results in increased relatedness, inbreeding, loss of genetic diversity Dispersal = ?gene flow No dispersal = NO gene flow To assess the impacts of forest fragmentation on population processes in key marsupial species
  • 14. ARC Linkage Conservation genetics and socio-ecology of marsupials in fragmented populations of south-eastern South Australia: towards a regional biodiversity management plan A/Prof Sue Carthew, Dr Steve Cooper, Dr Andrea Taylor PARTNERS: To assess the impacts of forest fragmentation on population processes in key marsupial species
  • 15. Fragmentation case studies Factors affecting population connectivity in fragmented landscapes: • Age of regrowth forest • Surrounding matrix • Habitat shape, edge effects • Lemurs, bird spp., gorillas, pademelons, bats, reptiles, frogs Sugar gliders (Mansoureh Malekien) • Restricted gene flow among some patches • Effects greater in small patches isolated by pine • Evidence for inbreeding in one patch from parentage analysis Yellow-footed antechinus (Amanda McLean) • Some evidence of differentiation between populations • Higher relatedness among females within patches than in continuous forest
  • 16. Common ringtail possum • Nocturnal arboreal marsupial • Broad distribution, abundant in a variety of forest habitats • Generalist herbivore – leaves, flowers, seeds of eucalypt spp., acacia spp. • Can build dreys • Survives in degraded habitats, found in fragmented landscapes
  • 17. Study site 10 23 11 21 18 30 10 35 23 20 47 7 23 15 78 43 74
  • 18. Data collection Site selection based on: • patch size • distance to neighbouring patch (0.5- >10 km) • 3 sites within continuous forest (distances between sites comparable) • 251 possums patches within pine • 189 possums patches within agriculture • 48 from 3 continuous forest sites • Genotyped at 15 microsatellites • Analysed for genetic diversity and genetic differentiation
  • 19. 1. Genetic Diversity Have possums in patches retained genetic diversity? • HH and L sig. Lower allelic richness and heterozygosity • Larger patches levels comparable to continuous forest • Trend towards lower H and AR in ag patches YES for some, NO for others, not related to patch size alone
  • 20. 2. Population structure Do possums move through the pine? • Five distinct clusters identified from 8 populations sampled  • No sub-structure within continuous forest  • HH and L genetically isolated  • P a subset of continuous forest  • SG, W and HS virtually same cluster membership  Yes, but pine hinders dispersal and gene flow Less dispersal into small, isolated patches
  • 21. 2. Population structure Do possums move through paddocks and roadside vegetation? 8 distinct genetic clusters identified Significant pop structure and isolation Limited evidence of gene flow/dispersal
  • 22. Pop Differentiation HH HS L P REN SG W WD HH HS 0.05 L 0.19 0.12 P 0.11 0.03 0.17 REN 0.10 0.03 0.13 0.00 SG 0.08 0.03 0.12 0.03 0.04 W 0.06 0.04 0.14 0.05 0.07 0.04 WD 0.09 0.02 0.13 0.02 0.02 0.03 0.05 BG G HC M PS RR SQ REN BG G 0.08 HC 0.08 0.07 Population pair-wise FST shows all M 0.06 0.04 0.08 pops except P and R as significantly PS 0.04 0.08 0.11 0.05 RR 0.08 0.11 0.09 0.08 0.09 different (most p < 0.0001) SQ 0.07 0.05 0.07 0.02 0.06 0.07 REN 0.03 0.04 0.06 0.03 0.04 0.05 0.03 Patches vs Continuous R1 R2 R3 No sig difference between R1 and R2 R1 0.12 <0.0001 (2.5 km) R2 0.007 <0.01 Sig. Differentiation of R3 from other R3 0.038 0.033 patches (3 km)
  • 23. Dispersal patterns • Mammalian patterns of dispersal – Sex-biased – Males disperse as juveniles or young adults – Females philopatric • In fragmented landscapes these patterns may be disrupted if movement is inhibited • Use genetic relatedness to look at patterns
  • 24. PINE PADDOCKS P and SG not sig Males Males 0.600 0.300 0.400 0.200 0.100 0.200 Mean 0.000 r 0.000 U -0.100 -0.200 L -0.200 -0.400 BG G HC M PS RR SQ HH HS L P SG W WD Females Females 0.800 0.300 0.600 0.200 0.400 0.100 r 0.200 0.000 0.000 -0.100 -0.200 -0.200 HH HS L P SG W WD BG G HC Patch M PS RR SQ Patch Continuous Forest All others sig. higher relatedness than 0.300 0.200 expected by chance 0.100 Mean Both sexes show this trend r 0.000 U -0.100 L -0.200 R1 M R2 M R3 M R1 F R2 F R3 F cf continuous forest neither females or Patch males show this pattern
  • 25. Summary • Intervening matrices appear to hinder dispersal and gene flow of possums – Less problematic in larger patches than smaller ones – Larger patches have comparable genetic diversity to continuous forest – Smaller patches HH and L show signatures of genetic isolation through low heterozygosity and lower allelic diversity. • Findings of lower dispersal in both sexes in fragments important implications for social structure and mating system • Pastoral land has greater impact on ringtail possums – Depend on several factors • Patch size • Age of pine • Distance to neighbouring patch • Time since isolation
  • 26. Recommendations and What next? – Modelling – which factors affect connectivity – position/distance/ size of patch but need to quantify – Incorporate landscape features – roadside vegetation, plantations, grazed remnant vegetation. Circuitscape (uses algorithms from electronic circuit theory to predict patterns of dispersal) – Incorporate more species • Corridors to join patches on the periphery of landscapes • Multiple potential sources of immigration important for genetic diversity • Continued conservation of large patches that can support viable populations to maintain remaining communities
  • 27. Acknowledgements Field volunteers for valuable Australian Research Council Linkage assistance with possuming Grants Scheme, with partners: • Department for the Environment and Heritage Martin Pepper for providing • Forestry SA photographs • Hancock Victorian Plantations • Nature Foundation of South Kathy Saint for assistance Australia with microsatellite development • South Australian Museum
  • 28. The Environment Institute Where ideas grow Next Seminar: 27 November Professor Kym Anderson Regional implications of climate change for the Australian wine industry