BioEnergy Research

, Volume 8, Issue 2, pp 471–481 | Cite as

Bioenergy Feedstocks at Low Risk for Invasion in the USA: a “White List” Approach

  • Lauren D. Quinn
  • Doria R. Gordon
  • Aviva Glaser
  • Deah Lieurance
  • S. Luke Flory
Article

Abstract

Proposed introductions of non-native bioenergy feedstocks have resulted in disagreements among industry, regulators, and environmental groups over unintended consequences, including invasion. Attempting to ban or “black list” known or high probability invasive species creates roadblocks without offering clear alternatives to industry representatives wishing to choose low invasion risk feedstocks. Therefore, a “white list” approach may offer a proactive policy solution for federal and state agencies seeking to incentivize the cultivation of promising new feedstocks without increasing the probability of non-native plant invasions in natural systems. We assessed 120 potential bioenergy feedstock taxa using weed risk assessment tools and generated a white list of 25 non-native taxa and 24 native taxa of low invasion risk in the continental USA. The list contains feedstocks that can be grown across various geographic regions in the USA and converted to a wide variety of fuel types. Although the white list is not exhaustive and will change over time as new plants are developed for bioenergy, the list and the methods used to create it should be immediately useful for breeders, regulators, and industry representatives as they seek to find common ground in selecting feedstocks.

Keywords

Biofuel Energy crop Invasive plant Weed risk assessment White list 

Introduction

In an effort to meet alternative energy mandates set by the 2007 Energy Independence and Security Act, bioenergy companies are investing in novel and, in many cases, non-native feedstocks that promise high yields on unproductive land [1]. However, these feedstocks can share key traits with invasive plant species, including high rates of establishment, rapid biomass accumulation, and the ability to thrive in low resource environments [2, 3]. Furthermore, current estimates suggest that dedicated energy crops could be planted on over 60 million hectares in the USA [4], potentially providing an immense propagule load [5] from production sites and along transport routes. Although several of the proposed feedstocks present relatively low invasion risk [6, 7, 8, 9, 10, 11], the prevailing message from ecologists and environmental groups has been highly precautionary [12, 13]. Such a precautionary approach may be justified, considering that over 90 % of all economically and ecologically damaging invasive plant species are thought to have originated from intentional introductions [14, 15, 16, 17, 18, 19, 20, 21].

Concerns about invasion risk are increasingly highlighted in the regulation of new feedstocks at the state and federal levels. For example, public outcry over invasion risk, in part, prompted the US Environmental Protection Agency (EPA) to adopt new standards to prevent escape by the approved feedstocks Arundo donax (giant reed) and Pennisetum purpureum (elephant/napier grass) [13, 22]. In addition, in the 2014 Farm Bill, congress strengthened an earlier provision that prohibits the US Department of Agriculture (USDA) from supporting potentially invasive feedstocks through its Biomass Crop Assistance Program (BCAP) [23]. At the state level, Florida (F.S.A. § 581.083) and Mississippi (Miss. Code Ann. § 69-25-10) have enacted laws that require permitting and bonding of non-native bioenergy plantations to mitigate invasion risk [24, 25]. In Oregon, the state agriculture department requires permits and containment practices for A. donax plantations and has restricted areas where the species can be cultivated (OAR 603-052-(1206-1250)). In addition, state and federal noxious weed regulations must be consulted prior to feedstock selection [11, 26]. Avoidance of noxious weeds is not sufficient to prevent invasion, however, since these lists poorly represent invaders outside cultivated areas [27, 28] and likely omit incipient invaders that are established in low numbers.

Regulation of invasive species directly affects bioenergy companies, particularly when large investments are made in the development of feedstocks that are later deemed problematic by regulators. For example, the company that petitioned for A. donax to be approved as a new fuel pathway has been forced to delay commercialization for over 2 years due to the unexpected requirement for risk mitigation planning and documentation (D. Richardson, Chemtex Group, personal communication, 2014). Although market factors such as profitable biomass yields are likely to dominate decisions regarding feedstock selection, there is interest from industry in using low invasion risk feedstocks that will avoid delays in approval and the responsibility for introducing potentially invasive species (J. Klingenberg, Repreve Renewables, LLC, personal communication, 2014). Existing risk assessment literature largely emphasizes the dangers of high-risk feedstocks, however, and provides few useful alternatives. Instead of creating a “black list” of prohibited high-risk feedstocks, a “white list” of low invasion risk feedstocks offers a positive approach for both companies and government agencies and could be used to fast-track approval of or reduce liability for producers using low-risk feedstocks. An example of a white list for bioenergy feedstocks already exists in the State of Florida (Non-native Species Planting Permits [5B-57.011]), where taxa produced for food, forage, or fiber, and those considered to have a low risk for invasion are white-listed and can be exempted from the state’s permitting requirements [23]. This approach is intended to incentivize the use of non-invaders in Florida. Here, we offer an initial white list of low invasion risk native (indigenous to the USA) and non-native feedstocks, extending Florida’s approach to the continental USA. Of note is that our list is based solely on invasion risk and does not evaluate other potential ecological concerns associated with bioenergy feedstocks.

Creating a White List of Low Invasion Risk Feedstocks for the USA

To generate a feedstock white list with taxa representing a diversity of growth habits, industrial uses, and climates, we first compiled a database of vascular feedstocks being used or considered for bioenergy production. We identified 120 candidate taxa (Table 1) that were mentioned as feedstocks in state and federal government documents and databases [26, 27, 28 FL Rule 5B-57.011], environmental and industry groups’ white papers [4, 10, 11, 26, 29, 30, 31], feedstock-related books [32], and primary literature on invasion potential of bioenergy crops, including existing invasion risk assessment papers on the subject [6, 7, 8, 9, 33, 34].
Table 1

All taxa considered for a biofuel white list, with Australian Weed Risk Assessment (WRA) conclusions (i.e., low risk, evaluate further, or high risk), scores (possible range −14 to 29); see text for score cutoff points for each conclusion), and literature sources, in square brackets. *Denote conclusions made after secondary screening (see text for further explanation)

Taxon

Conclusion

Agave spp.

US native

Aleurites moluccana

Low risk (6*[75]), evaluate (3*) [76], high risk (12) [38]

Andropogon gerardii

US native

Arachis glabrata

Low risk (−11 [76] −1 [38])

Arachis hypogaea

Low risk (−2 [38])

Arundo donax

High risk (11 [6, 8], 12 [38], 19 [78])

Arundo formosana

Evaluate (5[46])

Attalea speciosa

Low risk (−2 [39])

Azadirachta indica

High risk (10 [38])

Beta vulgaris ssp. vulgaris convar. saccharifera

Low risk (−6 [38])

Brassica juncea

High risk (15 [38])

Brassica napus

High risk (16 [38])

Brassica rapa; syn. B. campestris

Low risk (4* [39])

Calotropis gigantea

High risk (15 [38])

Calotropis procera

High risk (8 [46], 15 [38])

Camelina sativa

Low risk (4* [39]), High risk (9.5 [38])

Cannabis sativa

High risk (8.5 [38], 11.5 [7])

Casuarina equisetifolia

High risk (11 [75], 15 [7], 21 [38], 23 [78])

Chrysopogon zinzanioides (fertile); syn. Vetiveria zizanioides

High risk (9 [38])

Chrysopogon zinzanioides var. “Sunshine” (sterile); syn. Vetiveria zizanioides

Low risk ( −9 [39],−8 [38])

Cocos nucifera

Low risk (−4 [38], −3 [75])

Coffea arabica

Low risk (−3 [75]), High risk (1* [78], 2* [38])

Copaifera langsdorffii

Evaluate (4* [38])

Crotalaria juncea

Evaluate (1* [38]), High risk (7 [39])

Cuphea viscosissima

US native

Diospyros virginiana

US native

Diospyros kaki

High risk (1* [78])

Elaeis guineensis

High risk (8 [75], 9 [7], 10 [38])

Eucalyptus amplifolia

Low risk (−2 [39], 0 [9]), evaluate (2* [8])

Eucalyptus camaldulensis

High risk (12 [8], 18 [9], 19 [39])

Eucalyptus dorrigoensis

Low risk (−4 [39], −3 [9])

Eucalyptus dunnii

Low risk (−3 [39], −2 [9], 0 [38])

Eucalyptus globulus

High risk (10 [38], 18 [9])

Eucalyptus grandis

High risk (8 [8], 9 [39], 10 [9], 11 [38])

Eucalyptus gunnii

Low risk (1* [39], 2* [9]), evaluate (2* [38])

Eucalyptus macarthurii

Evaluate (6* [9])

Eucalyptus nitens

Low risk (0 [39], 1* [9])

Eucalyptus robusta

Low risk (−1 [75], 3* [38]), high risk (11 [9])

Eucalyptus saligna

High risk (7 [38], 9 [39])

Eucalyptus smithii

Low risk (1* [9])

Eucalyptus torelliana

Evaluate (4* [38]), high risk (13 [9])

Eucalyptusurograndis” (E. urophylla × grandis)

Low risk (1* [38]), evaluate (3* [39], 4* [9])

Eucalyptus urophylla

Low risk (4* [38], 6* [77]), evaluate (6* [7]), high risk (7 [9])

Eucalyptus viminalis

High risk (9 [39], 10 [9])

Euphorbia lathyris

High risk (8 [7], 9 [38])

Festuca arundinacea

High risk (17 [38])

Fraxinus uhdei

High risk (11 [38])

Gleditsia triacanthos

US native

Glycine max

Low risk (−3 [7])

Gossypium barbadense

Evaluate (5* [38])

Gossypium hirsutum

High risk (9 [38])

Gynerium sagittatum

High risk (13 [39])

Helianthus annuus

US native

Hordeum vulgare

Low risk (0 [75])

Ipomoea batatas

Low risk (2* [38])

Jatropha curcas

High risk (11 [80], 17 [38], 19 [8])

Lespedeza cuneata

High risk (17 [38])

Lesquerella fendleri

US native

Leucaena leucocephala

High risk (11 [80], 15 [38], 21 [8], 26 [78])

Linum usitatissimum

High risk (9.5 [38])

Liriodendron tulipifera

US native

Macadamia integrifolia

Low risk (−1 [38])

Maclura pomifera

US native

Manihot esculenta

Low risk (3* [38])

Milletia pinnata; syn. Pongamia pinnata

High risk (7 [38], 9 [7])

Miscanthus × giganteus

Low risk (−9 [8], −7 [6])

Miscanthus sacchariflorus

High risk (20 [39])

Miscanthus sinensis

High risk (14 [76])

Moringa oleifera; syn. M. pterygosperma

Low risk (1* [38]), high risk (9 [39])

Morus alba

Evaluate (2.5* [79])

Oenothera spp.

US native

Olea europaea

Evaluate (2 [80])

Olea europaea ssp. cuspidata

High risk (11 [38])

Olea europaea ssp. europaea

Evaluate (5* [38])

Panicum maximum; syn. Urochloa maxima

High risk (17 [38])

Panicum virgatum

US native

Paraserianthes falcataria

High risk (8 [7])

Paulownia elongata

Low risk (−1 [38], 6* [39])

Paulownia tomentosa

Evaluate (4* [74]), high risk (7 [80], 9 [38], 14 [39])

Pennisetum purpureum

High risk (10 [80], 16 [38], 18 [8, 78])

Pennisetum purpureum × glaucum

Evaluate (5* [39])

Perilla ocymoides

High risk (14 [39])

Persea americana

Low risk (0 [75], 3* [38])

Phalaris arundinacea

High risk (25 [39])

Pinus echinata

US native

Pinus elliottii

US native

Pinus palustris

US native

Pinus radiata

US native

Pinus taeda

US native

Pittosporum resiniferum

Evaluate (6* [38])

Platanus occidentalis

US native

Populus spp.

US native

Prosopis juliflora

High risk (19 [38])

Prosopis spp.

US native

Psidium cattleianum

High risk (16 [75], 18 [38])

Pueraria montana var. lobata

High risk (9 [80], 24 [38])

Quercus acutissima

Evaluate (2* [39])

Ricinus communis

High risk (8 [80], 9 [78], 21 [38], 24 [8])

Robinia pseudoacacia

US native

Rubus fruticosus

High risk (29 [39])

Saccharum hybrid L 79-1002

Low risk (−1 [39])

Saccharum arundinaceum

Low risk (3* [8])

Saccharum officinarum

Low risk (−2 [38], 5* [8]), high risk (5* [78])

Saccharum spontaneum

High risk (17 [38], 19 [39])

Salix spp.

US native

Sesbania grandiflora

Low risk (2* [38]), high risk (10 [39])

Simmondsia chinensis

US native

Sorghastrum nutans

US native

Sorghum bicolor “grain sorghum” syn. S. vulgare

Low risk (6* [38]), evaluate (3 [80]), high risk (7 [39])

Sorghum bicolor “shattercane”

High risk (17.5 [38], 18 [39])

Sorghum bicolor “sweet”

Low risk (3* [8])

Sorghum halepense

High risk (25 [80])

Spartina spp.

US native

Thlaspi arvense

High risk (19 [38])

Thysanolaena latifolia

High risk (11 [39])

Triadica sebifera; syn. Sapium sebiferum

High risk (14 [38], 18 [76])

Triticum aestivum

Low risk (3* [74])

Ulex europaeus

High risk (20 [38], 26 [80])

Zea mays

Low risk (−1 [74]), evaluate (2 [46])

Ziziphus mauritiana

High risk (9.5 [38], 12 [80])

Continental US natives (noted in conclusion column) and low-risk taxa with known industrial uses for bioenergy were retained in our white list and are found with additional information in Table 2. Note that Eucalyptus amplifolia has two scores from the same group of authors (references [8, 9]); the later conclusion (“low risk (0 [9])”) reflects a reanalysis prompted by additional data that were not available for the earlier assessment (“evaluate (2* [8])”). Sources of WRA scores and conclusions are noted by numbers inside the brackets as listed in the “Reference” section. Where references in individual papers cite the same scores as are available on on-line databases [8, 9, 12], the databases are cited as they make available the full WRA results

We did not include algae in the database, despite examples of biofuel development from algae in the USA [35, 36, 37], because we are unaware of an invasion risk assessment tool for non-vascular species. Although we sought to make the list comprehensive, the rapid development of the industry means that it should not be considered static or exhaustive. Additionally, not all of these taxa will meet the industry’s yield or profitability demands in all regions of the continental USA

After compiling our database of potential feedstocks, we consulted the weed risk assessment literature and public databases [including 38, 39, 40] to identify the invasion risk level associated with each taxon of interest. Although a small number of demographic and climate models have been completed to predict potential invasion of bioenergy feedstocks [41, 42, 43, 44], we selected the Australian Weed Risk Assessment (WRA) system as the basis of our white list. This WRA has proven accuracy (>90 %) in predicting major invaders across a range of geographies [45, 46, 47], and unlike other types of predictive models, results for a large number of species are accessible in public databases. For example, many of the taxa in our database have existing cultivation histories for food, forage, or fiber, which increases the data on which risk assessment could be based. The WRA defines specific score thresholds that differentiate taxa predicted to have a low probability (≤0) from those with high probability (≥7) of becoming invasive. Intermediate scores (1–6) indicate taxa requiring further evaluation before risk can be determined [46]. Species receiving this latter outcome may be run through an additional screening tool [48], which has been consistently demonstrated to resolve the risk for a large proportion of species with intermediate scores [45].

Regardless of the geographic focus of the test, WRA scores for species often result in consistent conclusions of high or low risk [49]. An explicit test of the accuracy of scores generated in other regions for risk assessment in Singapore resulted in the conclusion that WRA scores are transferrable to new geographies with similar environmental conditions [47]. Given the broad range of environmental conditions within the continental USA, we included all available WRA scores for our study, including scores generated specifically for the USA as well as those focused on other locations worldwide. However, using scores from any new US-based WRAs would benefit future iterations of the white list, particularly if the white list is adapted for use in specific US regions or states.

To encourage the selection of native feedstocks wherever possible, we automatically included taxa native to the continental USA (24 of the 120 species identified) on the white list (Table 2). The use of native genotypes within their native range reduces the risk of escaped plants having negative impacts in recipient native communities, especially relative to non-native taxa [50], whose impacts can be less predictable. Low risk non-natives (n = 25) were also placed on the white list. Taxa receiving high risk scores (≥7) or listed on the federal noxious weeds list (e.g., Rubus fruticosus and Saccharum spontaneum) [51] were not considered for the white list (Table 1). Several species received WRA scores between 1 and 6 (“evaluate further”). Where use of the secondary screen [48] resulted in a low risk determination, the taxon was included on the white list; otherwise, it was removed from further consideration pending data availability to resolve the risk category.
Table 2

“White list” of native and low-risk non-native taxa for feedstock development in the USA

Feedstock

Common name

Industrial uses

Preferred climate

US Nativity

Source

Agave spp.

Agave

EtOH

Arid temp

Southwest, but varies with species. A. sisalana invasive in Southeast

DOE (2013)

Andropogon gerardii

Big bluestem

EtOH, BD, comb

Temp

Continental USA except ID, NV, WA, OR, CA, and HI

DOE BTU (2011); DOE (2013)

Arachis glabrata

Rhizoma peanut

BD

Temp, subtr

Non-native

Buddenhagen et al. (2009)

Arachis hypogaea

Peanut

BD

Temp, subtr

Non-native

GISP (2007)

Attalea speciosa syn. Orbignya barbosiana

Babassu palm

BD

Subtr, trop

Non-native

Sanford et al. (2009)

Beta vulgaris

Sugar beets

EtOH

Temp, subtr

Non-native

DOE BTU (2011); Halford et al. (2010)

Brassica rapa

Field mustard

BD

Temp

Non-native

DOE BTU (2011)

Chrysopogon zinzanioides var. “Sunshine”; syn. Vetiveria zizanioides var. “Sunshine

Vetiver grass

EtOH

Subtr

Non-native

FLDACS (2013)

Cocos nucifera

Coconut palm

EtOH, comb

Trop, subtr

Non-native

Buddenhagen et al. (2009); GISP (2007); Sanford et al. (2009)

Cuphea viscosissima

Blue waxweed

BD

Temp, subtr

Eastern USA: Mid-Atlantic, Southeast, lower Midwest, and eastern plains

Sanford et al. (2009)

Diospyros virginiana

Persimmon

EtOH, comb

Temp

Continental USA except north-central, northwest, and most of southwest

GISP (2007)

Eucalyptus amplifolia

Cabbage gum

EtOH, comb

Subtr

Non-native

Gordon et al. (2011 & 2012)

Eucalyptus dorrigoensis

Dorrigo white gum

EtOH, comb

Subtr

Non-native

FLDACS (2013); Gordon et al. (2012)

Eucalyptus dunnii

Dunn’s white gum

EtOH, comb

Subtr

Non-native

FLDACS (2013); Gordon et al. (2012)

Eucalyptus nitens

Shining gum

EtOH, comb

Subtr

Non-native

FLDACS (2013); Gordon et al. (2012)

Eucalyptus smithii

Gully gum

EtOH, comb

Subtr

Non-native

FLDACS (2013); Gordon et al. (2012)

Gleditsia triacanthos

Honey locust

EtOH, comb

Temp

Continental USA except WA and OR

GISP (2007)

Glycine max

Soybean

EtOH

Temp

Non-native

Buddenhagen et al. (2009); DOE BTU (2011); EPA (2011); GISP (2007); Halford et al. (2010); Sanford et al. (2009)

Helianthus annuus

Sunflower

BD

Temp

Continental USA; use with caution: NOXIOUS In IA

Buddenhagen et al. (2009); DOE BTU (2011); GISP (2007); Halford et al. (2010); Sanford et al. (2009)

Hordeum vulgare

Barley

EtOH

Temp

Non-native

DOE BTU (2011)

Ipomoea batatas

Sweet potato

EtOH

Temp, subtr, trop

Non-native

GISP (2007)

Lesquerella fendleri

Fendler’s bladderpod

BD

Temp, subtr

AZ, CO, KS, NM, OK, TX, and UT

Sanford et al. (2009)

Liriodendron tulipifera

Tulip or yellow poplar

EtOH, comb

Temp

Eastern USA

DOE (2013)

Macadamia integrifolia

Macadamia nut

BD

Trop, subtr

Non-native

Buddenhagen et al. (2009)

Maclura pomifera

Hedge apple/osage orange

BD

Temp, subtr

Continental USA except MN, ND, MT, WY, ID, NV, and AZ

GISP (2007)

Manihot esculenta

Cassava

EtOH

Trop, subtr

Non-native

GISP (2007)

Miscanthus × giganteus (sterile)

Giant Miscanthus (“Illinois”)

EtOH, comb

Temp, subtr

Non-native

Low et al. (2008); Barney et al. (2008); DOE BTU (2011); EPA (2011); GISP (2007); Gordon et al. (2011); Halford et al. (2010)

Oenothera spp.

Evening primrose

BD

Temp

Varies with species

Sanford et al. (2009)

Panicum virgatum

Switchgrass

EtOH, comb

Temp

Continental USA except WA, OR, CA, and HI

Barney et al. (2008); Buddenhagen et al. (2009); DOE BTU (2011); DiTomaso et al. (2007); DOE (2013); EPA (2011); GISP (2007); Halford et al. (2010)

Paulownia elongata

Paulownia

comb

Temp

Non-native

FLDACS (2013)

Persea americana

Avocado

BD

Trop, subtr

Non-native

Buddenhagen et al. (2009)

Pinus echinata

Shortleaf pine

EtOH, comb

Subtr

Mid-Atlantic, Southeast, portions of the Midwest and plains

DOE BTU (2011)

Pinus elliottii

Slash pine

EtOH, comb

Subtr

AL, FL, GA, LA, MS, NC, SC, and TX

DOE BTU (2011)

Pinus palustris

Longleaf pine

EtOH, comb

Subtr

AL, AR, FL, GA, LA, MS, NC, SC, TX, and VA

DOE BTU (2011)

Pinus radiata

Monterey pine

EtOH, comb

Subtr

CA

DOE (2013)

Pinus taeda

Loblolly pine

EtOH, comb

Subtr

Southeast and south central USA

DOE BTU (2011)

Platanus occidentalis

American Sycamore

EtOH, comb

Temp

Eastern USA

DOE (2013)

Populus spp.

Cottonwood/poplar

EtOH, comb

Temp

Varies with species

Low et al. (2008); DOE BTU (2011); DOE (2013); Halford et al. (2010)

Prosopis spp.

mesquite

EtOH, comb

Subtr

Southwest, but varies with species

GISP (2007)

Robinia pseudoacacia

Black locust

EtOH, comb

Temp

Mid-Atlantic and southern Midwest; use with caution: NOXIOUS in MA, invasive in 12 states

DOE (2013)

Saccharum “L 79-1002” hybrid*

Hybrid sugarcane

EtOH

Trop, subtr

Non-native

FLDACS (2013)

Saccharum arundinaceum

Hardy sugarcane

EtOH

Trop, subtr

Non-native

Gordon et al. (2011)

Salix spp.

Willow

EtOH, comb

Temp

varies with species

Low et al. (2008); DOE BTU (2011); Halford et al. (2010)

Simmondsia chinensis

Jojoba

BD

Temp

CA, AZ, and UT

Buddenhagen et al. (2009); Sanford et al. (2009)

Sorghastrum nutans

Indian grass

EtOH, comb

Temp

Continental US except ID, NV, WA, OR, CA, and HI

DOE BTU (2011)

Sorghum bicolor “sweet”

Sweet sorghum

EtOH

Temp, subtr

Non-native

DOE (2013); Gordon et al. (2011)

Spartina spp.

Cordgrass

EtOH

Temp

Varies with species; use with caution: some spp. are invasive

Low et al. (2008)

Triticum aestivum

Wheat

EtOH

Temp

Non-native

DOE BTU (2011); GISP (2007); Halford et al. (2010)

Zea mays

Corn

EtOH

Temp

Non-native

DOE BTU (2011); EPA (2011); Halford et al. (2010); Sanford et al. (2009)

Neither the list of species nor industrial uses (BD biodiesel, comb combustion, EtOH ethanol) should be considered exhaustive. Preferred climates (subtr subtropical, temp temperate, trop tropical) are listed to assist in siting potential production areas. Source of native region was the USDA NRCS PLANTS database [59]. Reference to a species as “invasive” in the US Nativity column is derived from such a designation on state or regional invasive plant council lists; reference to a “noxious” designation denotes that the species is regulated and prohibited in certain states. Any genotype of a species included in this white list that is known to be invasive is not recommended for use

The data we used were based on WRAs conducted on non-native taxa at the species level unless specific hybrids, cultivars, or other subspecific taxa with sufficient trait data were identified. Many novel genotypes, including hybrids, cultivars, and genetically modified organisms, are being developed or are already available as feedstocks [e.g., 52]. Such taxa may have traits that reduce or increase invasion potential compared to the parent species (e.g., sterile vs. fertile varieties of Miscanthus × giganteus (giant Miscanthus) and sterile vs. fertile cultivars and hybrids of Pennisetum purpureum [53, 54]. While the proprietary nature of taxa developed for commercial purposes often limits the data available for WRA at subspecific levels, the risk assessment process can and should be modified for such taxa [e.g., see 39, 55] when data become available.

In many cases (n = 48), we found multiple scores for the same species, assessed by different sources. Different scores can result from application of the WRA in different geographies, inclusion of data not available when earlier assessments were conducted, or differences in interpretation of the WRA [45]. In 33 % of those cases (16/48), the risk conclusions from multiple sources were inconsistent. In those cases, we did not include the species on our white list, even if one source concluded that the species was low risk. We made the single exception to this rule for Zea mays (corn or maize), because of its long-term cultivation without evidence of invasive tendencies [56]. Further data are needed to resolve the risk category for species with conflicting results.

Understanding the White List

Feedstocks with low invasion risk status and favorable agronomic properties will be most attractive to the bioenergy industry. Our white list (Table 2) offers 49 native and non-native low-risk options that will meet these requirements across much of the USA (e.g., Panicum virgatum (switchgrass)) or in more specific “niche” growing conditions (e.g., Agave spp. (agave) in the arid southwest). Table 2 also indicates the sources that mention the bioenergy potential of each taxon. Those taxa associated with a greater number of sources or with more industry-relevant sources (e.g., Department of Energy (DOE)) are likely to be the taxa with the strongest potential for government support and the greatest potential returns on investment. These include Glycine max (soybean), Helianthus annuus (wild sunflower), sterile Miscanthus × giganteus, Panicum virgatum, native Populus spp. (poplar), Sorghum bicolor “sweet” (sweet sorghum), and Zea mays.

Native plants bred for bioenergy production and grown in monoculture outside of their native range carry some of the same invasion and impact risks as non-natives [2, 57, 58]. Therefore, we provide the native region (Table 2; derived primarily from the USDA’s PLANTS database [59]) and stress that native genotypes should be grown only in those states or regions to avoid any unintended ecological impacts resulting from escape. Examples exist of species or biotypes that are invasive outside of or even within their native regions in the USA [60, 61]. For example, Helianthus annuus is native to the entire continental USA but is listed as a noxious weed in Iowa and was found to be a high risk species in Hawaii (WRA score = 10.5 [7]). In addition, several native taxa or close relatives on our list are known invaders elsewhere, including Hawaii, so it is important to reemphasize that the current list is intended to provide low-risk solutions for the continental USA only. For example, native Pinus elliottii (slash pine) spreads spontaneously to uncultivated areas on at least two continents [62] and received high risk scores for New Zealand and Great Britain [63] and an “evaluate further” outcome for Hawaii [38]. Genera with native members (e.g., Populus spp.) appear on the white list with the assumption that producers will grow only native genotypes and only within their native regions. For many of the non-native species on our list, climate-matching models are unavailable for the USA. Therefore, potential production regions will have to be tested and assigned based on relatively broad estimates of each taxon’s preferred climate (see Table 2).

Further Safeguards

White list taxa are predicted to have low invasion risk but are not guaranteed to remain low-risk in changing climates or as novel genotypes are developed through traditional breeding or genetic modification. For example, several companies are near commercialization of fertile Miscanthus × giganteus feedstocks, which are likely to pose greater invasion risk than the sterile hybrid on our white list [6, 34, 44, 64]. Rather than potentially increasing invasion risk by inducing fertility, plant breeders could introduce traits to minimize potential escape, including sterility, indehiscence or non-shattering of propagules, or reduced brittleness of perennating vegetative structures [34, 65]. Varieties of Sorghum bicolor sweet, for example, naturally allocate more photosynthate to sugars than to starch and to stem than seed tissues, resulting in lower risk of invasion than Sorghum bicolor “grain” or the highly invasive Sorghum bicolor “shattercane” [56]. Similarly, the fertile wild-type of Chrysopogon zizanioides (syn. Vetiveria zizanioides; vetiver grass) is invasive, but the sterile “Sunshine” genotype from southern India has low invasion risk [38]. Regardless of the type of “improvement,” any and all novel genotypes of white listed species, including native species, would require new assessments before being added to future iterations of the list. In addition, new assessments should be completed prior to any planned relocation or expansion of production regions. For example, the recent spatial shifts in USDA Hardiness Zones [http://www.ars.usda.gov/is/pr/2012/120125.htm] demonstrate that climate changes are likely to influence the future distributions of both native and non-native taxa.

A set of specific management practices, including monitoring and eradication of any off-site colonization, should also be developed for all feedstocks grown commercially—even those on the white list. The USDA’s BCAP program has set a precedent for the requirement of such practices for a low-risk feedstock (sterile Miscanthus × giganteus) [66]. We concur with other authors in recommending similar requirements at the state and/or federal levels [25] and encourage industry to voluntarily adopt safeguards to prevent escape in advance of regulatory changes [23, 67]. Management practices should be applied at all stages of bioenergy production–from planting through processing—and may include timing harvests to minimize spread of seeds, maintaining clean equipment, using closed transportation systems to transfer feedstocks to processing facilities, and putting an eradication plan into place before production [26, 68].

Policy Implications

This white list offers a starting point to guide policies at the federal and/or state levels, potentially reducing emerging conflicts among agencies that support bioenergy and those that manage invasive species. Inconsistencies in recommendations among federal agencies risk violating Executive Order 13112 [69], which explicitly requires integration and consistency of invasive species policy at the federal level [23]. For example, A. donax has been assessed as a high-risk species by the USDA Plant Epidemiology and Risk Analysis Laboratory [70], and the USDA Agriculture Research Service is working to identify an effective biological control agent to manage invasions [71]. However, A. donax has been approved for cultivation under the Renewable Fuel Standard implemented by EPA [22], highlighting the fact that conflicts among agencies and with the Executive Order have not been resolved. The non-governmental Invasive Species Advisory Committee (ISAC) has recommended that inconsistencies in federal policy related to invasiveness and biofuels be identified and addressed and that the federal government take steps to minimize the risk of bioenergy feedstocks becoming invasive, including evaluating candidate feedstocks and promoting low-risk taxa [4]. The use of a white list can allow agencies to fast-track taxa that have been assessed as low-risk.

A clear liability regime is needed to reduce incentives for using high-risk bioenergy feedstocks by assigning negligence liability to feedstock producers for damages from and remediation of invasions by bioenergy feedstocks [10, 27, 28]. Policy approaches should reduce potential liability for producers using white-listed feedstocks cultivated under specific management practices to further reduce invasion risk. These actions would be evidence that due diligence was practiced even in the unlikely event that feedstocks escape and become harmful invaders.

Conclusion

The invasion risk-based white list we have created for the USA contains 49 taxa representing a wide variety of growth habits, harvestable yields, favored climates, agronomic traits, and cultivation practices. The white list approach not only provides producers with clearly identified low invasion risk options, but it additionally can and should be used in federal and state policy to incentivize the use of low invasion risk feedstocks [25]. Use of taxa from the white list may reduce conflicts between objectives for increasing renewable fuel production and reducing unintended impacts and costs resulting from propagation of invasive plants. Additionally, because a small proportion of the species we examined require further evaluation or had conflicting results, future investigation may augment the list relatively quickly. To reduce the potential for biomass feedstocks to become invasive, we recommend that prior to major investment and commercialization, all potential bioenergy feedstocks be screened with science-based tools as we have done here [28, 57], tested experimentally for invasion risk [28, 53], and reassessed regularly [39] as novel genotypes are developed and as climate change shifts potential production regions. All of these processes should be stipulated in state and federal statutes and regulations [25].

Here, we have focused on invasion risk, but other unintended environmental, economic, and health impacts of bioenergy crops should not be discounted. For example, while some Eucalyptus species pose a low risk for invasion [9], their high productivity is accompanied by high water use, which may have unintended impacts in water-limited systems[72, 73]. These additional considerations should be used to refine geographic and management criteria for bioenergy crop cultivation.

Notes

Acknowledgments

This concept was developed during a December 2012 meeting on legislative and policy tools to address the risks posed by potentially invasive bioenergy feedstocks. We thank the host organizations (National Wildlife Federation and University of Illinois) and the participants for their perspectives and insights. Aimee Cooper assisted with completion of risk assessments. Comments from B. Endres and J. Sibbing improved the manuscript. We also acknowledge funding support from the Energy Biosciences Institute, the Doris Duke Charitable Foundation, the Florida Chapter of The Nature Conservancy, the University of Florida Dean for Research and Dean for Extension, the Florida Department of Agriculture and Consumer Services, and the Florida Fish and Wildlife Conservation Commission.

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Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Lauren D. Quinn
    • 1
  • Doria R. Gordon
    • 2
  • Aviva Glaser
    • 3
  • Deah Lieurance
    • 4
  • S. Luke Flory
    • 5
  1. 1.Energy Biosciences InstituteUniversity of IllinoisUrbanaUSA
  2. 2.The Nature Conservancy, Department of BiologyUniversity of FloridaGainesvilleUSA
  3. 3.National Wildlife FederationWashingtonUSA
  4. 4.Center for Aquatic and Invasive PlantsUniversity of Florida/IFASGainesvilleUSA
  5. 5.Agronomy DepartmentUniversity of FloridaGainesvilleUSA

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