Encroaching and Invasive C4 Grasses of South Texas Associate with and Potentially Alter Arbuscular Mycorrhizal Fungi Communities

Home , Bothriochloa ischaemum, Pappophorum

 Largest % of global land cover › > 50% ice free terrestrial landscape › Multi-continental range

 Perennial native grasslands › Very IMPORTANT  Ecologically picgrassland.jpg  Economically

2  North American perennial grassland › 3,200km North – South  Southern Canada – Texas › Rocky Mountains – 800km East › ~1.3 million km2

en.wikipedia.org

3  Ecological services › Wildlife habitat

› CO2 sequestration › Soil nutrient addition › Aquifer recharge  Human used products › Food › Fuel › Fiber

4  Habitat loss › Row crop agriculture › Urbanization

 Climate change creedyassociates.com › Alters ecosystem function

 Habitat degradation › Ecological invasion mobjectivist.blogspot.com  Encroaching and Invading species

5  Process by which: › New species enters a community  Native or Exotic species  Accidental or on purpose  3 Stages

› Arrival dec.ny.gov

› Establishment

fortybeads.com › Spread  Lockwood et al. 2007 blog.tavelpod.comr

6  Research concentrations › Recruitment limitation › Aboveground traits

 Belowground ????? › Little known

 Above- and belowground communities › Intrinsically linked › Regulate ecosystem-level processes

7  Arbuscular mycorrhizal fungi (AMF)  Nematodes  Bacteria

 Beneficial  Harmful › Mineral solubilization › Parasitic › Fixing nitrogen › Pathogenic › Access to other soil resources

8  ~70% of all vascular plant species  Hyphae greatly increase the absorbing surface area  4-20% of plant photosynthate consumed by its AMF

Hyphae

Drawing by N. C. Johnson Arbuscules Photo by Joe Morton

9  Nutrient uptake

 Plant growth rate

 Soil nutrient pools

 Drought tolerance

 Resistance to root pathogens

10 GROWTH RESPONSE (%)

SPECIES - 25 % 0 % 25 % 50 % 75 % 100 % Andropogon gerardii Sorghastrum nutans Schizachyrium scoparium Panicum virgatum Bothriochloa bladhii Bouteloua curtipendula Buchloe dactyloides Elymus cinereus Bromus inermis Bouteloua gracilis Pascopyrum smithii Agrostis stolonifera C4 Koeleria macrantha C3 Poa pratensis

Wilson and Hartnett 1998 11  Van der Putten (2007) › Majority of exotic species are non-mycorrhizal › Functionally distinct from the native flora

 In the Great Plains the exotic species

introduced resemble the dominant C4 native species in physiological and functional traits

12 Bever, J. D. ,1997; 2003

13  Negative › Slowed the rate of population growth › Increased or stabilized diversity › Prominent in native systems  Positive › Increased rate of species growth

› Decreased species diversity Bever, J. D. ,1997 › Resulting in mono-specific stands

Bever, J. D. 1994; 1997; 2002; 2003

15 16  Invading native grasslands › Reduce plant biodiversity

› Reduce or alter wildlife biodiversity  Hickman et al. 2006

› Restoration concerns  Multiple trophic levels  Multiple spatial scales

17  Old World Bluestem (OWB) › Perennial warm – season grass  Introduced in 1917 › Europe, Asia, and Russia

 Erosion control inspection.gc.ca  Increase forage  Central and Southern Great Plains › Millions of acres › Marginal farmlands › Road side right – of – ways  Harmoney and Hickman 2004 18  Temporary benefit › Unpalatable after maturity  Escaped original plantings › Invading native prairies › Rapid expansion  “Creating moving fronts” ca.uky.edu  OWB better competitors › Greater biomass  Schmidt et al. 2008 › Hinder native seedlings  Wilson et al. 2012

ca.uky.edu

19 Non-Sterile + Mycorrhizal fungi

Non-Sterile Sterile + Mycorrhizal fungi - Mycorrhizal fungi Sterile - Mycorrhizal fungi

Native: Big Bluestem Andropogon gerardii

Exotic: Old World Bluestem

Bothriochloa sp. 20 AM Root Colonization

10 AM AM (%) Root Colonization

0 NP OWB NP OWB NP OWB NP OWB

W. KS E. KS W. OK E. OK

Soil Source NP = Soil Collected from Native Prairie OWB = Soil Collected from under Old World Bluestem

21 AM Soil Hyphal Abundance Determined by Fatty Acid Analyses 25

10 nmol/g soil 5

0 NP OWB NP OWB NP OWB NP OWB

W. KS E. KS W. OK E. OK

Soil Source NP = Soil Collected from Native Prairie OWB = Soil Collected from under Old World Bluestem

22 Invasive/Encroaching C4 grasses in South Texas

Pennisetum ciliare Dichanthium annulatum Heteropogon contortus Buffelgrass Kleberg Bluestem Tanglehead

Photos from South Texas Natives

23 Collaborative project with Texas A & M Kingsville and South Texas Natives

24  Determine if dominant native and invasive

C4 grasses of S. Texas are mycorrhizal dependent.

 Determine if invasive C4 grasses alter plant- soil-microbial feedbacks and limit native grass establishment and growth.

 Determine if addition of native soil amendments improve establishment and growth of native grasses. 25  5 reps › For each species x soil source x soil treatment

Native plant species: Invasive/encroaching species: • Hooded windmillgrass • Tanglehead Chloris cucullata Heteropogon contortus •Arizona Cottontop •Buffelgrass Digitaria californica Pennisetum ciliare •Pink Pappusgrass • Kleberg Bluestem Pappophorum bicolor Dichanthium anulatum • Plains Bristlegrass Setaria leucopila

26 Soil source: • Native Prairie • Beneath Tanglehead (encroaching) • Beneath Buffelgrass (invasive) • Beneath Kleberg Bluestem (invasive) Soil treatments: • Field soil (soil left nonsterile) • Field soil with native prairie soil inoculum added • Steamed (steam-pasteurized) • Steamed with native prairie soil inoculum added

Harvested after 14 weeks: • Quantified above- and belowground biomass

27 Pappophorum bicolor Pink Pappusgrass

450

400

350

300

250

200

150

Total Plant Biomass (g) Biomass Plant Total 100

0 STEAMED STEAMED STEAMED STEAMED S+INNOC S+INNOC S+INNOC S+INNOC FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FS +INNOC FS FS +INNOC FS FS +INNOC FS

Native Prairie Soil H. contortus D. annulatum P. ciliare

28  AMF Dependent:  Non-AMF Dependent: › Pappophorum bicolor › Chloris cucullata  Pink Pappusgrass  Hooded Windmillgrass › Seteria vulpiseta › Pennisetum ciliare  Plains Bristlegrass  Buffelgrass › Heteropogon contortus  Tanglehead  AMF Facultative: › Dichanthium annulatum  Kleberg Bluestem › Digitaria californica  Arizona Cottontop

flickriver.com 29 30 31 Seteria vulpiseta Plains Bristlegrass

400

350

300

250

200

150

100 Total Plant Biomass (g) Biomass Plant Total

0 STEAMED STEAMED STEAMED STEAMED S+INNOC S+INNOC S+INNOC S+INNOC FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FS +INNOC FS FS +INNOC FS FS +INNOC FS

Native Prairie Soil H. contortus D. annulatum P. ciliare

32 Chloris cucullata Hooded Windmillgrass

400

350

300

250

200

150

100 Total Plant Biomass (g) Biomass Plant Total 50

0 STEAMED STEAMED STEAMED STEAMED S+INNOC S+INNOC S+INNOC S+INNOC FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD FS +INNOC FS FS +INNOC FS FS +INNOC FS

Native Prairie Soil H. contortus D. annulatum P. ciliare

33 Pappophorum bicolor Pink Pappusgrass

450

400

350

300

250

200

150

Total Plant Biomass (g) Biomass Plant Total 100

0 STEAMED STEAMED STEAMED STEAMED S+INNOC S+INNOC S+INNOC S+INNOC FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD SOIL FIELD FS +INNOC FS FS +INNOC FS FS +INNOC FS

Native Prairie Soil H. contortus D. annulatum P. ciliare

34  Invasive/encroaching exotic grasses › Have varied reliance on AMF  As did the natives › Exert differential effects on native grasses  Alteration of AMF community  Use of native soil amendments may hold potential  But where do we get this soil for large projects?  May be other mechanisms at work

35 Pappophorum bicolor Pink Pappusgrass

450

400

350

300

250

200

150

Total Plant Biomass (g) Biomass Plant Total 100

0 STEAMED STEAMED STEAMED STEAMED S+INNOC S+INNOC S+INNOC S+INNOC FIELD SOIL FIELD FIELD SOIL FIELD FIELD SOIL FIELD SOIL FIELD FS +INNOC FS FS +INNOC FS FS +INNOC FS

Native Prairie Soil H. contortus D. annulatum P. ciliare

36 37  Assess effects of yellow bluestem (Bothriochloa ischaemum) extractions on germination, survival, and growth of native grasses.  Big bluestem (Andropogon gerardii)  Little bluestem (Schizachyrium scoparium)

 Assess effects of yellow bluestem leaf litter on survival and growth of native grasses.

38  Ha1: Yellow bluestem leachate will reduce germination of native grasses, with no conspecific effects.

 Ha2: Yellow bluestem leachate or litter will reduce biomass production of native grass seedlings, with no conspecific effects.

 Ha3: Yellow bluestem leachate or litter will reduce the survivorship of native grass species, with no conspecific effects.

 Ha4: Big bluestem leachate or litter will have no conspecific or heterospecific effects.

39  Germination study:  For each species (8 Reps): • 50 seeds were placed into a petri dishes • 5 ml added to each dish • Yellow bluestem leachate (invasive) • Big bluestem leachate (native) • Deionized water (control) • Percent germination was determined • Every 3 days for 21 days

40 Survivorship and growth study:  For each species (8 replicates): • One seedling per pot • Containing 1 kg native soil • 60 mL added • Initiation and every other week • Yellow bluestem leachate (invasive) • Big bluestem leachate (native) • Deionized water (control) • 20 mm of leaf litter • Applied at initiation • Yellow bluestem leaf litter (invasive) • Big bluestem leaf litter (native) • No litter application (control) • Percent survival determined after 8 weeks • Biomass dried and weighed at 8 weeks 41 120

100

60 BB Leachate YB Leachate

40 Germination (%) Percent of Control

0 Big Bluestem Little Bluestem Yellow Bluestem

42 4

3.5

2.5

Control 2 BB Lechate YB Leachate 1.5 Aboveground Biomass (g) 1

0.5

0 Big Bluestem Little Bluestem Yellow Bluestem

43 0.6

0.5

0.4

0.3 BB Litter YB Litter

Aboveground Biomass (g) 0.2

0.1

0 Big Bluestem Little Bluestem Yellow Bluestem

44 120

100

60 BB Leachate YB Leachate

40 Seedling Survival (%) Percent of Control 20

0 Big Bluestem Little Bluestem Yellow Bluestem

45 120

100

60 BB Litter YB Litter

40 Seedling Survival (%) Percent of Control 20

0 Big Bluestem Little Bluestem Yellow Bluestem

46  Yellow bluestem leachate profoundly reduced the germination of native seeds, with no conspecific effects.  Yellow bluestem leachate and leaf litter significantly reduced the survivorship of native seedlings.

47  Big bluestem leachate had little effect on native or invasive species.  Big bluestem litter reduced biomass production of all species compared to no litter controls; greater reductions were observed with yellow bluestem litter.  Big bluestem litter did not reduce seedling survivorship of any species; yellow bluestem litter profoundly reduced native species survivorship.

48  Soil treatments showed no differences › EC (soil salinity) or pH  Leachates showed only one difference › Native leachate had greater phenolic content  Native systems = negative feedbacks

tolweb.org Bever 2003

49  Invasion may be driven by: › Alterations of AMF community › Use of allelopathic biochemicals › May be a synergistic effect

 Need for species by species management  Future research › Assess soil microbial community change  Pyro-sequencing › Biochemical identification 50  Restoration recommendations: › Use of native soil addition  Restore native soil community  Again where do we get the soil? › Negate allelopathic compounds  Determine residency time of compounds › Organic matter addition  Aid in restoring soil chemistry  Increase restoration success  Restore ecosystem function www.konza.ksu.edu 51 52  OWB invasion › Diverse grasslands vs. monospecific stands

 Loss of plant biodiversity

 Loss of wildlife biodiversity › Alteration of:  Habitat structure  Habitat composition  Available resources

53  Previous work: › Cool – season exotics  Schwartz and Whitson 1987  Hayslett and Danielson 1994 › OWB monocultures in Texas  Sammon and Wilkins 2005  Found lower small mammal: › Diversity › Richness › Abundance / Relative abundance

54  Small mammals › Vital to grassland ecosystems  Seed dispersers  AMF spore dispersers  Primary consumers

www2.ljworld.com  Objectives: › To determine if grasslands invaded by OWB contain similar small mammal communities as native grasslands. › Determine the vegetative characteristics causing any observed differences.

55 56  2 treatments  4 Transects › 20 traps/transect  Sherman live traps  20m spacing › >200m between transects  2 years › 4 seasons/year › 4 days/season › 2 checks/day

57  Visual obstruction › Robel pole  Litter Depth  Vegetative Composition › 1m2 frame virtualbirder.com  Modified Daubenmire class method › Forb, grass, bare ground, etc › Native vs. OWB  Aerial cover › Elevated Daubenmire  5cm, 10cm, 25cm, 50cm

hosho.ees.hokudai.ac.jp 58 Native B. ischaemum +Native Species + Litter Depth + Native Species 5cm + B. ischaemum + Native Species 10cm + B. ischaemum 5cm + B. ischaemum 10cm + B. ischaemum 25cm

59  5120 total trap days › 24 hrs in 1 day

Species Actual Captures Species Native OWB Deer Mouse 101 36 Cotton Rat 74 237 Elliot's Short-tailed Shrew 3 10 Fulvous Harvest Mouse 4 1 Prairie Vole 4 7 Hispid Pocket Mouse 1 0 Eastern Harvest Mouse 4 1 White-footed Mouse 2 2 TOTAL 193 294 60 10.00

9.00

8.00

7.00

6.00

5.00 Richness 4.00

3.00

2.00

1.00

0.00 Native OWB

61 70.00

60.00

50.00

40.00 Native

30.00 OWB

20.00 Relative Abundance (%)

10.00

0.00 Cotton rat Deer Mouse Elliot Short-tailed Prairie Vole Shrew

62 63 64  Cotton rat › Increased aerial predator avoidance  Major source of mortality

 Deer mice

› Increased foraging efficiency vet.osu.com  Lower seed recovery in thick litter/vegetation  Smaller body size

Realanimallife.com 65  Native grasslands › Higher species richness › Higher relative abundances of deer mice

 OWB invaded grasslands › Higher relative abundances of cotton rats

 Vegetative structure showed few differences › May be due to 40-60% invasion vs. monoculture

66  OWB invasion leads to: › Fewer species › Greater abundances of these species

 Promote early eradication of OWB › 60% invasion saw only minor shifts › Lag in small mammal community shift

 Increased fire frequency may maintain native habitat structure › Greater ecological concerns

67  Invasive species = BIG PROBLEM › Economic Concerns  $35 billion cost to control or in lost product › This does not cover cost of restoration

 Restoration of invaded lands is complex › Focus has been on above ground BUT… › Current projects show belowground can be just as or even more important

 Invasion may be driven by: › Alterations of AMF community › Use of allelopathic biochemicals › May be a synergistic effect › May be more complex  Tangled web!

 Early control and restoration can limit impacts

 Need for more research 69 Funding: OSU- Natural Resource Ecology and Management Texas A & M Kingsville: Tim Fulbright Caesar Kleberg Wildlife Research Institute South Texas Natives David Davidson Konza Prairie Biological Station NSF -LTER Fort Hays State University K-State Hays Ag Experiment Station: Keith Harmoney USDA Range Research Program

Project Support: Stuart Wilson (OSU – PSS) Chris Stansberry (OSU – SRR) Dr. David Lalman – OSU – Animal Science TX A & M Kingsville Graduate Student: Eric Grahmann OSU Graduate Students: Shubha Shrestha, Morgan Noland, Eric Duell, Stephanie Grischkowsky, and many others Numerous undergraduate research assistants Numerous Volunteers (OSU – TWS) 70