Bandicoots in the ’burbs Creating healthy soil microbial communities for tree health and ecosystem function

Trish Fleming, Natasha Tay, Janine Kuehs, Shannon Dundas, Anna Hopkins, Gillian Bryant, Katinka Ruthrof, Leonie Valentine, Treena Burgess, Brett Brenchly, Bonnie Beal Richardson, Giles Hardy Role of fauna in ecosystems • Herbivores – Plant cover /richness – Fuel loads • Pollinators – Plant recruitment – Plant richness • Predators – Regulate prey abundances – Regulate herbivores • Dispersal agents – Plant & fungi distribution • Bioturbators – Physically rearrange soils and sediments Biodiversity hotspot = biodiversity threatened Biodiversity hotspot = biodiversity threatened Digging mammals are ecosystem engineers

100% 90% 80% 70% 60% IUCN 50% status 40% Least concern

30% Not threatened

20% Data deficient

10% Vulnerable

0% Endangered No (131 Yes (29 Critically spp) spp) endangered Extinct Digger? Loss of distribution range for digging mammals Fleming et al. 2014

Current distribution Historical distribution

. Short-beaked echidna Common wombat S. hairy-nosed wombat

dae N. hairy-nosed wombat Vombati Long nosed Echymipera Long nosed bandicoot E. barred bandicoot Desert bandicoot† W. barred bandicoot Lesser bilby† Greater bilby

Peramelidae S. brown bandicoot N. brown bandicoot Golden bandicoot Pigfooted bandicoot† Long-nosed Potoroo Broad-faced Potoroo† Long-footed Potoroo Gilbert's Potoroo Desert Rat-kangaroo† Northern Bettong

Potoroidae Woylie Boodie Southern Bettong Rufous Bettong

. Numbat

S. marsupial mole * . N. marsupial mole * 0% 50% 100% % of Australian land mass The quenda Isoodon fusciventer • Australian marsupial (Family Peramelidae) – Predominantly nocturnal – 1-2 kg (~1.5kg) – Home range: 2–5 ha The quenda Isoodon fusciventer Valentine et al. 2013 • Omnivores - forage for subterranean food – Small conical shaped pit (7 – 10 cm) – Extrapolates to ~3.9 tonnes of soil per year The quenda Isoodon fusciventer Mycophagous specialists (potoroos, bettongs and bandicoots) forage for hypogeous fungi, which form 50-90% of their diet Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016

1. ↑ SOIL TURNOVER ↑ Soil heterogeneity

Soil mechanical properties, e.g. •texture •structure SPOIL HEAP •density •erosion PIT

Altered chemical properties •bring nutrients to soil surface Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016 0.012 1.2 1.35 1.4 1.5 1.5 40 Body mass (kg) 1. ↑ SOIL

TURNOVER wombat

↑ Soil heterogeneity bandicoot

Eastern barred Pebblemound mouse Woylie Quenda *Greater bilby *Boodie N. hairy-nosed body body mass)

Soil mechanical 1.8 Annual turnover soil 2.5 3.6 2.4

properties, e.g. (tonnes / individual / kg •texture 20 20 14 •structure SPOIL HEAP •density •erosion PIT

Altered chemical properties •bring nutrients to soil surface Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016

2. ↑ ORGANIC MATTER

↑ Debris locked into soil SPOIL HEAP Resources for soil biota • ↑ soil biota PIT • ↑ nutrients • ↑ soil health

↑ Nutrient cycling

Fires cooler Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016

UNDUG SPOIL HEAP

3.↑ WATER PIT INFILTRATION & SOIL MOISTURE

Break down the hydrophilic surface • ↑ water infiltration • ↑ erosion Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016

4. ↑ SEED RETENTION & PLANT RECRUITMENT

↑ Seed numbers • Seed caching • ↑ Seed capture • ↓ Seed predation (due to burial) SPOIL HEAP ↑ seedling germination & PIT recruitment

↑ plant growth ↑ plant species richness & diversity

Changed plant community composition & structure Fleming et al. 2014, Digging mammals are ecosystem engineering species Valentine et al. 2013, 2016

5.↑ FUNGAL DISPERSAL & RECRUITMENT

↑ Mycorrhizal fungi SPOIL HEAP ↑ tree access to nutrients (e.g. P, N) PIT ↑tree productivity & recruitment

↑ soil exploration by trees

↑ tree resistance to pathogens Brundrett & Tedersoo (2018) Mycorrhizal symbioses WA

e.g. UK Valentine et al. (2018) Mycorrhizal symbioses • Higher incidence of fungal hyphae in dug soil Mycorrhizal symbioses

Dispersal of fungi

Food source Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures Karakamia (AWC) 275 hectares fenced 1994

1km

Perup (DBCA)

420 hectares fenced 2010

1km Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures ? Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures • intact soil cores collected from within 1m of the base of marri trees • planted with marri seeds • grown in a glasshouse for 5 months • seedlings were harvested • roots subjected High Throughput Sequencing for mycorrhizal fungi • Compared relative differences in abundance and diversity of fungi Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures • Marri seedlings grew significantly larger on soils taken from inside enclosures

F1,56=17.36, p<0.001 0.7

0.6

0.5

0.4

0.3

Log(Shoot weight; g) weight; Log(Shoot 0.2

Site 0.1 K I O Site Treatment P Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures

F1,56=3.03, p=0.087 • Site differences in 1040 fungal abundance 1030 1020 1010 1000 990 980 970 960 950

Number of fungi present fungi of Number 940 Site 930 K I O Site • Marked differences in Treatment P ectomycorrhizal fungi associations (2-way PERMANOVA)

– Inside/outside fence: F1,55=2.42, p<0.001

– Site: F1,55=4.23, p<0.001 Dundas et al. (2018) 1. Comparison between inside and outside predator-proof exclosures

Karakamia more outside the fence | more inside the fence Pezizaceae Pezizomycota Ectomycorrhizal fungi Rhulandiella sp Russulaceae ECM Sebacinaceae Sebacinales

Tomentella sp A Arbuscular mycorrhizal fungi M Glomeraceae Dothideomycetes Saprotrophs Flagelloschypha sp Galerina sp Helotiaceae Hyaloschyphaceae Leohumicola sp Mycena sp saprotroph Oiodendron sp Phomopsis sp Pleosporales Sordariomycetidae Chaetomium sp

Microscopic saprotrophs ph Chaetothyriales yeast?

Saprotro Coniochaetales -0.05 -0.03 -0.01 0.01 0.03 0.05 0.07 0.09 Difference in abundance 2. Quenda scats as an inoculant for trees • Since 1990s, there has been a decline in tuart health in Yalgorup National Park – 80% mature trees have died – Potential causes: land clearing, decreased rainfall, inappropriate fire regimes, reduction in water table, insects, pathogens Hopkins et al. (In prep.) 2. Quenda scats as an inoculant for trees • Quenda scats contain a wide variety of fungal material

Backyards Urban Bushland Natural Bushland

ECM Truffle

ECM Sequestrate

ECM Other macro

Saprotroph macro

Lichen

Chytrid Hopkins et al. (In prep.) 2. Quenda scats as an inoculant for trees • 60 scats -> 826 fungal molecular operational taxonomic units (MOTUs) • Top 151 MOTUs identified = 91.3% of all sequence reads • 72 form large fruiting bodies (57.6% reads) • One Russula species represented 13% of all sequence reads • 8 known truffle species, 20 known mushrooms/cups

Russula Taxon Percentage Russula sp.1 13% Russula sp.2 2% Descomyces angustisporus 3% 15 Boletales combined 10% 16 Agaricales combined 9%

* Other orders were represented by <10% of all reads. Descomyces (augustisporus) • Fewer MOTUs closer to urbanisation (Rs=-0.348, p<0.001) • Less fungal diversity in diet closer to urbanisation (F2,18=51.67, p<0.001) Tay et al. (2018) 2. Quenda scats as an inoculant for trees

Russula

Cortinarius

Boletales (Austroboletus) Tay et al. (2018) 2. Quenda scats as an inoculant for trees

Inoculant Scats Scats Scats Scats Inoculant Scats Scats Scats Scats Mycorrhiza Mycorrhiza Mycorrhiza Mycorrhiza Smith et al. (current work) 2. Quenda scats as an inoculant for trees 3. Backyard Bandicoots - City of Mandurah Bryant et al. (2017) 3. Backyard Bandicoots - City of Mandurah 3. Backyard Bandicoots - City of Mandurah • Total number of bandicoot digs in quadrat, categorised by: 1. none (0 digs) 2. some (1 - 30 digs) 3. many (>30 digs) • Broad habitat survey in each location (10 x 10 m quadrat): – % canopy cover – Vegetation condition score (excellent, good, ok, poor, or urban park) • Dogs: allowed or not allowed on reserve • Further habitat information (5 x 5 m quadrat): – % bare ground – % leaf litter 106 study locations – % vegetated (<1m vegetation Included urban parks, estuary height) foreshore areas, vegetated reserves, and small and large bush pockets Bryant et al. (2017) 3. Backyard Bandicoots - City of Mandurah FUTURE WORK Can we identify mycorrhizal fungi? FUTURE WORK Can we restore ecosystem function by strategic translocations?

• Australian ecosystems have undergone a massive loss of ecosystem processes relatively recently • Effects of these losses may yet be felt – e.g. reduced growth, flowering, seed set, no recruitment FUTURE WORK Can we restore ecosystem function by strategic translocations?

Increase Trap leaf water litter & infiltration other (therefore soil organic moisture) matter

Increased microbial activity

Increased soil nutrient cycling More seedlings recruited Improved vegetation resilience and growth Thanks Michael Bretz, Hannah Anderson, Lara Osborne, Bryony Palmer, Judy Gardner, Barbara Wilson, Nicole Willers, Bill Bateman, David Ford Photos: Narelle Dybing, Judy Dunlop, Bill King, Leonie Valentine, Shannon Dundas

HOLSWORTH RESEARCH ENDOWMENT