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Earthworms as Eco-engineers in theRestoration of Oil and Brine-Impacted Soils Following Remediation
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Earthworms as Eco-engineers in the Restoration of Oil and Brine-
Impacted Soils Following RemediationNitya AlahariKerry Sublette
Eleanor JenningsCenter for Applied Biogeosciences
University of TulsaGreg ThomaDuane Wolf
University of ArkansasKathleen Duncan
University of OklahomaTim Todd
Kansas State UniversityMac A. Callaham, Jr.USDA-Forest Service
Project Objective:Accelerated Restoration of Oil- and
Brine-impacted Sites• Both the original spill and the remediation
process disrupt soil ecology– Disruptions in N and P cycling– Reduced diversity of soil organisms– Loss of vegetation
• All levels of ecosystem affected– Producers– Consumers– Decomposers
Project Summary• Objective: to determine the efficacy of the introduction of non-
indigenous earthworms to accelerate the restoration of remediated oil and brine spill sites
• Original treatments to be investigated included all combinations of the following plus no treatment:– inoculation with Eisenia fetida– fertilizer addition – hay cover
• Treatments were applied in enclosures designed to retain E. fetida and exclude other macrofauna.
• Within 60 days:– earthworms indigenous to the area were detected in significant
numbers both outside and inside of the enclosures – very few E. fetida could be found.
• Thus all enclosures were accessible to indigenous earthworms and in reality there were only four treatments: hay + fertilizer (HF), hay only (H), fertilizer only (F), and no treatment (N).
• The greatest earthworm activity was assumed to occur in those enclosures where there was food (surface hay)
Metrics Used to Evaluate Treatments
• Soil nutrients• Microbial biomass as PLFA
– PLFA = phospholipid fatty acid analysis• N-cycling bacteria• Nematode numbers and community structure• No acceptable metric for earthworm numbers was
identified– Earthworms were observed but were not confined to the
enclosures; therefore, direct counts were unreliable– Earthworm castings were damaged when the layer of damp
decomposing hay was removed to expose the surface in HF and H treatments
Block 1 Block 2 Block 3 Block 4
Original Experimental Design – Brine Site
(Similar layout at Hydrocarbon Site)
Worms + Hay + Fertilizer
Worms + Hay
Worms + Fertilizer
Hay + Fertilizer
Worms
Hay
Fertilizer
No Treatment
Project Timeline• Ripped and tilled sites• Installed earthworm enclosures and added
amendments (fertilizer and/or hay)• Inoculated with Eisenia fetida
– 5 worms per enclosure per worm treatment• Initial conditions:
– 350-600 mg/kg Na+ in brine site– 9,500-16,000 mg/kg total extractable hydrocarbons in
hydrocarbon site• Sampling:
– August 2005– October 2005– June 2006
Filling enclosure with homogenized soil at hydrocarbon site
Filling earthworm enclosure with homogenized soil
Hay
Earthworm enclosures installed and amendments added at hydrocarbon site
Entire site covered with hay for moisture and temperature control
Earthworm Observations• At the first sampling, earthworms were found in the top 15 cm of most
enclosures– A. trapezoides– Diplocardia sp.– Very few E. fetida
• Most worm observations at soil moisture concentrations of 22-26%
0
2
4
6
8
10
12
16-18 18-20 20-22 22-24 24-26 26-28 28-30 30-32
Percent Moisture
No.
of O
bser
vatio
ns o
f W
orm
s
Brine SiteHydrocarbon site
TreatmentBrine Site
August 2005 October 2005 June 2006
HF 26.0 ± 2.1 23.3 ± 2.8 29.4 ± 3.3
H 25.7 ± 3.3 24.2 ± 3.4 29.2 ± 2.9
F 26.1 ± 1.6 22.5 ± 3.0 25.9 ± 4.0
N 25.7 ± 1.6 21.9 ± 2.5 29.6 ± 3.3
NativePrairie
13.7 ± 1.5(n=4)
TreatmentHydrocarbon
Site
August 2005 October 2005 June 2006
HF 22.0 ± 3.8 18.9 ± 3.9 23.1 ± 6.4
H 21.7 ± 4.5 18.2 ± 4.6 23.2 ± 8.4
F 20.7 ± 4.3 19.3 ± 4.8 28.4 ± 13.3
N 18.2 ± 4.9 19.4 ± 4.1 21.3 ± 6.5
NativePrairie
13.5 ± 1.7(n=4)
Soil Moisture
Mean ± std. dev. with n=8 or 9 unless otherwise indicated
Sample Date
TreatmentBrine Site
NO3-Nmg/kg
NH4-Nmg/kg
P(mg/kg)
%N %C
August 2005
HF 1.65 ± 0.74 a 7.7 ± 4.8 a 11.7 ± 8.1 a 0.28 ± 0.53 a 1.51 ± 0.31 a
H 1.74 ± 0.69 a 14.6 ± 9.0 b 25.7 ± 19.6 ab 0.11 ± 0.03 a 1.69 ± 0.38 a
F 1.50 ± 0.55 a 6.5 ± 2.5 a 15.7 ± 17.6 ab 0.10 ± 0.008 a 1.51 ± 0.25 a
N 1.85 ± 1.04 a 12.5 ± 8.1 ab 34.5 ± 24.4 b 0.38 ± 0.72 a 1.45 ± 0.24 a
October 2005
HF 3.42 ± 1.37 a 2.78 ± 1.00 a 24.0 ± 12.5 a 0.12 ± 0.02 a 1.67 ± 0.25 a
H 4.21 ± 3.29 a 2.05 ± 0.97 a 6.4 ± 1.7 b 0.12 ± 0.008 a 1.57 ± 0.28 a
F 2.85 ± 0.67 a 2.52 ± 1.08 a 22.5 ± 10.7 a 0.11 ± 0.006 a 1.61 ± 0.30 a
N 4.95 ± 3.74 a 1.99 ± 1.14 a 6.8 ± 1.3 b 0.12 ± 0.007 a 1.54 ± 0.23 a
Brine Site Nutrients1,2
1 All values are mean ± std. dev. with n=8 or 92 Different letters following values for a given sample data indicate significant differences at p<0.05
Sample Date
TreatmentHydrocarbon
Site
NO3-N(mg/kg)
NH4-N(mg/kg)
P(mg/kg)
%N %C
August 2005
HF 12.1 ± 6.2 a 3.25 ± 0.57 a 89.2 ± 51.9 a 0.20 ± 0.01 a 3.63 ± 0.30 a
H 10.1 ± 6.0 a 3.20 ± 0.82 a 27.3 ± 7.1 b 0.19 ± 0.01 a 3.66 ± 0.30 a
F 18.7 ± 24.4 a 3.00 ± 0.33 a 69.2 ± 30.2 a 0.18 ± 0.008 a 3.51 ± 0.30 a
N 8.7 ± 7.2 a 2.72 ± 0.41 a 27.7 ± 11.5 b 0.19 ± 0.009 a 3.53 ± 0.25 a
October 2005
HF 6.6 ± 0.9 a 1.29 ± 0.24 a 66.4 ± 18.3 a 0.20 ± 0.01 a 3.68 ± 0.22 a
H 7.5 ± 4.4 a 1.41 ± 0.15 ab 22.9 ± 7.2 b 0.19 ± 0.01 a 3.62 ± 0.34 a
F 8.0 ± 3.9 a 1.62 ± 0.40 b 55.0 ± 13.7 a 0.20 ± 0.01 a 3.76 ± 0.33 a
N 5.4 ± 0.8 a 1.50 ± 0.34 ab 25.5 ± 9.5 b 0.19 ± 0.02 a 3.69 ± 0.20 a
Hydrocarbon Site Nutrients1,2
1All values are mean ± std. dev. with n=8 or 92Different letters following values for a given sample data indicate significant differences at p<0.05
Soil Viable Biomass in Terms of Concentration of Phospholipids (pmoles/g)1
TreatmentBrine Site
August 20052 October 20052 June 20063
HF 8,315 ± 3,464 a 11,497 ± 3936 a 7,168
H 9,917 ± 4,863 a 12,843 ± 3790 a 5,686
F 7,126 ± 3,099 a 11,033 ± 4089 a 6,700
N 6,893 ± 1,483 a 11,038 ± 3111 a 7,827
NativePrairie
10,333
TreatmentHydrocarbon
Site
August 20052 October 20052 June 20063
HF 7,623 ± 1,356 a 9,301 ± 3082 a 10,270
H 8,489 ± 2,975 a 8,146 ± 1970 a 6,974
F 6,872 ± 2,339 a 7,577 ± 2751 a 6,929
N 7,270 ± 1,944 a 8,248 ± 3870 a 8,874
NativePrairie
23,718
2mean ±std.dev with n=8 or 9
3Eight-fold composite
1Concentration of phospholipids proportional to concentration of viable microbial biomass
Evaluation of Metrics
• Of all the metrics used to evaluate treatments, only one was capable of distinguishing between treatments –nematode numbers and community structure– Trophic groups– Colonizer-persister classes
Free-living NematodesBrine Site
HF H F N
Treatment
0
200
400
600
800
1000
1200
1400
1600
1800
2000
Free
-livi
ng N
emat
odes
(#/1
00 g
) August 2005 October 2005 June 2005
Maturity IndexBrine Site
HF H F N
Treatment
1.0
1.2
1.4
1.6
1.8
2.0
2.2
2.4
Mat
urity
Inde
x
August 2005 October 2005 June 2006
Brine SiteAugust 2005
HF H F N
Treatment
0
100
200
300
400
500
600
700
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Brine SiteOctober 2005
HF H F N
Treatment
0
20
40
60
80
100
120
140
160
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Brine SiteJune 2006
HF H F N
Treatment
0
100
200
300
400
500
600
700
800
900
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Free-living NematodesHydrocarbon Site
HF H F N
Treatment
0
200
400
600
800
1000
1200
1400
1600
1800
2000
Free
-livi
ng N
emat
odes
(#/1
00 g
) August 2005 October 2005 June 2006
Maturity IndexHydrocarbon Site
HF H F N
Treatment
1.0
1.2
1.4
1.6
1.8
2.0
2.2
2.4
Mat
urity
Inde
x
August 2005 October 2005 June 2006
Hydrocarbon SiteAugust 2005
HF H F N
Treatment
0
200
400
600
800
1000
1200
1400
1600
1800
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Hydrocarbon SiteOctober 2005
HF H F N
Treatment
0
200
400
600
800
1000
1200
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Hydrocarbon SiteJune 2006
HF H F N
Treatment
0
100
200
300
400
500
600
700
800
Nem
atod
es (#
/100
g)
Total Herbivores Total Microbivores Total Fungivores Total O/P
Preliminary Conclusions
• Indigenous earthworms quickly re-populate remediated oil and brine spill sites when hay and moisture are made available
• Nematode numbers and community structure – indicated more intense nutrient cycling in treatments that
included hay– sensitive metrics for assessing soil ecosystem restoration in
these sites• The availability of hay on the soil surface likely
correlates with earthworm activity